ERdj5 Is the ER Reductase that Catalyzes the Removal of Non-Native Disulfides and Correct Folding of the LDL Receptor

Molecular Cell

Volumn 50, Issue 6, 2013, Pages 793-804

  Oka, Ojore Benedict Valentine ^a   Pringle, Marie Anne ^a   Schopp, Isabel Myriam ^a   Braakman, Ineke ^b   Bulleid, Neil John ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; GLUCOSE REGULATED PROTEIN 78; LOW DENSITY LIPOPROTEIN RECEPTOR; OXIDOREDUCTASE; PROTEIN DISULFIDE ISOMERASE; PROTEIN ERDJ5; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOSOL; DISULFIDE BOND; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CELL LINE, TUMOR; CYSTINE; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTORS, LDL; RNA, SMALL INTERFERING;

MAMMALIA;

EID: 84880819436     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.05.014     Document Type: Article

References (34)

1. Alon A., Grossman I., Gat Y., Kodali V.K., DiMaio F., Mehlman T., Haran G., Baker D., Thorpe C., Fass D. The dynamic disulphide relay of quiescin sulphydryl oxidase. Nature 2012, 488:414-418.
2. Brown M.S., Goldstein J.L. Regulation of the activity of the low density lipoprotein receptor in human fibroblasts. Cell 1975, 6:307-316.
3. Bulleid N.J. Disulfide bond formation in the mammalian endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 2012, 4:4.
4. Bulleid N.J., Ellgaard L. Multiple ways to make disulfides. Trends Biochem. Sci. 2011, 36:485-492.
5. Chakravarthi S., Jessop C.E., Willer M., Stirling C.J., Bulleid N.J. Intracellular catalysis of disulfide bond formation by the human sulfhydryl oxidase, QSOX1. Biochem. J. 2007, 404:403-411.
6. Christianson J.C., Olzmann J.A., Shaler T.A., Sowa M.E., Bennett E.J., Richter C.M., Tyler R.E., Greenblatt E.J., Harper J.W., Kopito R.R. Defining human ERAD networks through an integrative mapping strategy. Nat. Cell Biol. 2012, 14:93-105.
7. Cormier J.H., Tamura T., Sunryd J.C., Hebert D.N. EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. Mol. Cell 2009, 34:627-633.
8. 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.
9. Dierks T., Dickmanns A., Preusser-Kunze A., Schmidt B., Mariappan M., von Figura K., Ficner R., Rudolph M.G. Molecular basis for multiple sulfatase deficiency and mechanism for formylglycine generation of the human formylglycine-generating enzyme. Cell 2005, 121:541-552.
10. Dong M., Bridges J.P., Apsley K., Xu Y., Weaver T.E. ERdj4 and ERdj5 are required for endoplasmic reticulum-associated protein degradation of misfolded surfactant protein C. Mol. Biol. Cell 2008, 19:2620-2630.
11. Durocher Y., Perret S., Kamen A. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 2002, 30:E9.
12. Ellgaard L., Ruddock L.W. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005, 6:28-32.
13. Gent J., Braakman I. Low-density lipoprotein receptor structure and folding. Cell. Mol. Life Sci. 2004, 61:2461-2470.
14. Groisman B., Shenkman M., Ron E., Lederkremer G.Z. Mannose trimming is required for delivery of a glycoprotein from EDEM1 to XTP3-B and to late endoplasmic reticulum-associated degradation steps. J.Biol. Chem. 2011, 286:1292-1300.
15. Hagiwara M., Maegawa K., Suzuki M., Ushioda R., Araki K., Matsumoto Y., Hoseki J., Nagata K., Inaba K. Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol. Cell 2011, 41:432-444.
16. Hatahet F., Ruddock L.W. Substrate recognition by the protein disulfide isomerases. FEBS J. 2007, 274:5223-5234.
17. Hosoda A., Kimata Y., Tsuru A., Kohno K. JPDI, a novel endoplasmic reticulum-resident protein containing both a BiP-interacting J-domain and thioredoxin-like motifs. J.Biol. Chem. 2003, 278:2669-2676.
18. Jansens A., van Duijn E., Braakman I. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 2002, 298:2401-2403.
19. Jessop C.E., Bulleid N.J. Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J.Biol. Chem. 2004, 279:55341-55347.
20. Jessop C.E., Chakravarthi S., Garbi N., Hämmerling G.J., Lovell S., Bulleid N.J. ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J. 2007, 26:28-40.
21. 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.
22. Jessop C.E., Watkins R.H., Simmons J.J., Tasab M., Bulleid N.J. Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J.Cell Sci. 2009, 122:4287-4295.
23. Jin Y., Awad W., Petrova K., Hendershot L.M. Regulated release of ERdj3 from unfolded proteins by BiP. EMBO J. 2008, 27:2873-2882.
24. Li Y., Lu W., Schwartz A.L., Bu G. Degradation of the LDL receptor class 2 mutants is mediated by a proteasome-dependent pathway. J.Lipid Res. 2004, 45:1084-1091.
25. Pena F., Jansens A., van Zadelhoff G., Braakman I. Calcium as a crucial cofactor for low density lipoprotein receptor folding in the endoplasmic reticulum. J.Biol. Chem. 2010, 285:8656-8664.
26. Riemer J., Appenzeller-Herzog C., Johansson L., Bodenmiller B., Hartmann-Petersen R., Ellgaard L. A luminal flavoprotein in endoplasmic reticulum-associated degradation. Proc. Natl. Acad. Sci. USA 2009, 106:14831-14836.
27. Ronzoni R., Anelli T., Brunati M., Cortini M., Fagioli C., Sitia R. Pathogenesis of ER storage disorders: modulating Russell body biogenesis by altering proximal and distal quality control. Traffic 2010, 11:947-957.
28. Schäuble N., Lang S., Jung M., Cappel S., Schorr S., Ulucan O., Linxweiler J., Dudek J., Blum R., Helms V., et al. BiP-mediated closing of the Sec61 channel limits Ca2+ leakage from the ER. EMBO J. 2012, 31:3282-3296.
29. Thomas C.G., Spyrou G. ERdj5 sensitizes neuroblastoma cells to endoplasmic reticulum stress-induced apoptosis. J.Biol. Chem. 2009, 284:6282-6290.
30. 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.
31. 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., et al. Loss of the oxidative stress sensor NPGPx compromises GRP78 chaperone activity and induces systemic disease. Mol. Cell 2012, 48:747-759.
32. Wilson R., Lees J.F., Bulleid N.J. Protein disulfide isomerase acts as a molecular chaperone during the assembly of procollagen. J.Biol. Chem. 1998, 273:9637-9643.
33. Wilson C.M., Farmery M.R., Bulleid N.J. Pivotal role of calnexin and mannose trimming in regulating the endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain. J.Biol. Chem. 2000, 275:21224-21232.
34. 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.