Different redox sensitivity of endoplasmic reticulum associated degradation clients suggests a novel role for disulphide bonds in secretory proteins

Biochemistry and Cell Biology

Volumn 92, Issue 2, 2014, Pages 113-118

  Medraño Fernandez, Iria ^a   Sitia, Roberto ^b   Fagioli, Claudio ^a   Otsu, Mieko ^a   Mezghrani, Alexandre ^c  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

Endoplasmic reticulum; Ero1; PDI; Protein degradation; Retro translocation

Indexed keywords

CELL MEMBRANES; CHAINS; SUBSTRATES; SULFUR COMPOUNDS;

ENDOPLASMIC RETICULUM; ERO1; PDI; PROTEIN DEGRADATION; RETRO-TRANSLOCATION;

PROTEINS;

DITHIOTHREITOL; MUTANT PROTEIN; PROTEIN DISULFIDE ISOMERASE; RIBOPHORIN I; SECRETORY PROTEIN;

ARTICLE; DISULFIDE BOND; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; OXIDATION; OXIDATION REDUCTION REACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; WESTERN BLOTTING;

ANIMALS; DISULFIDES; DITHIOTHREITOL; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; OXIDATION-REDUCTION; OXIDOREDUCTASES; PROTEIN DISULFIDE-ISOMERASES; PROTEINS;

EID: 84898081309     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/bcb-2013-0090     Document Type: Article

References (33)

1. Anelli T. Alessio M. Mezghrani A. Simmen T. Talamo F. Bachi A. Sitia R. 2002. ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family. EMBO J. 21 (4): 835-844. 10.1093/emboj/21.4.835. 11847130.
2. Anelli T. Alessio M. Bachi A. Bergamelli L. Bertoli G. Camerini S. et al 2003. Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J. 22 (19): 5015-5022. 10.1093/emboj/cdg491. 14517240.
3. Benham A.M. van Lith M. Sitia R. Braakman I. 2013. Ero1-PDI interactions, the response to redox flux and the implications for disulfide bond formation in the mammalian endoplasmic reticulum. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368 (1617): 20110403. 10.1098/rstb.2011.0403. 23530257.
4. Blais J.D. Chin K.T. Zito E. Zhang Y. Heldman N. Harding H.P. et al 2010. A small molecule inhibitor of endoplasmic reticulum oxidation 1 (ERO1) with selectively reversible thiol reactivity. J. Biol. Chem. 285 (27): 20993-21003. 10.1074/jbc.M110.126599. 20442408.
5. Cabibbo A. Pagani M. Fabbri M. Rocchi M. Farmery M.R. Bulleid N.J. Sitia R. 2000. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J. Biol. Chem. 275 (7): 4827-4833. 10.1074/jbc.275.7. 4827. 10671517.
6. de Virgilio M. Kitzmüller C. Schwaiger E. Klein M. Kreibich G. Ivessa N.E. 1999. Degradation of a short-lived glycoprotein from the lumen of the endoplasmic reticulum: the role of N-linked glycans and the unfolded protein response. Mol. Biol. Cell, 10 (12): 4059-4073. 10.1091/mbc.10.12.4059. 10588643.
7. Ellgaard L. Helenius A. 2003. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 48 (3): 181-191. 10.1038/nrm1052. 12612637.
8. Fagioli C. Sitia R. 2001. Glycoprotein quality control in the endoplasmic reticulum. Mannose trimming by endoplasmic reticulum mannosidase I times the proteasomal degradation of unassembled immunoglobulin subunits. J. Biol. Chem. 276 (16): 12885-12892. 10.1074/jbc.M009603200. 11278527.
9. Fagioli C. Mezghrani A. Sitia R. 2001. Reduction of interchain disulfide bonds precedes the dislocation of Ig-μ chains from the endoplasmic reticulum to the cytosol for proteasomal degradation. J. Biol. Chem. 276 (16): 40962-40967. 10.1074/jbc.M107456200. 11533039.
10. Fassio A. Sitia R. 2002. Formation, isomerisation and reduction of disulphide bonds during protein quality control in the endoplasmic reticulum. Histochem. Cell Biol. 117 (2): 151-157. 10.1007/s00418-001-0364-0. 11935291.
11. Fewell S.W. Travers K.J. Weissman J.S. Brodsky J.L. 2001. The action of molecular chaperones in the early secretory pathway. Annu. Rev. Genet. 35: 149-191. 10.1146/annurev.genet.35.102401.090313. 11700281.
12. Gillece P. Luz J.M. Lennarz W.J. de La Cruz F.J. Römisch K. 1999. Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerise. J. Cell Biol. 147 (7): 1443-1456. 10.1083/jcb.147.7.1443. 10613903.
13. Hagiwara M. Maegawa K. Suzuki M. Ushioda R. Araki K. Matsumoto Y. et al 2011. Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol. Cell, 41 (4): 432-444. 10.1016/j.molcel.2011.01. 021. 21329881.
14. Kopito R.R. 1997. ER quality control: the cytoplasmic connection. Cell, 88 (4): 427-430. 10.1016/S0092-8674(00)81881-4. 9038332.
15. Laboissiere M.C. Sturley S.L. Raines R.T. 1995. The essential function of protein-disulfide isomerase is to unscramble non-native disulfide bonds. J. Biol. Chem. 270 (47): 28006-28009. 10.1074/jbc.270.47.28006. 7499282.
16. Li Y. Camacho P. 2004. Ca2+-dependent redox modulation of SERCA 2b by ERp57. J. Cell Biol. 164 (1): 35-46. 10.1083/jcb.200307010. 14699087.
17. Lord J.M. Roberts L.M. Lencer W.I. 2005. Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr. Top. Microbiol. Immunol. 300: 149-168. 10.1007/3-540-28007-3-7. 16573240.
18. Magnuson B. Rainey E.K. Benjamin T. Baryshev M. Mkrtchian S. Tsai B. 2005. ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol. Cell, 20 (2): 289-300. 10.1016/j.molcel.2005.08.034. 16246730.
19. Mancini R. Fagioli C. Fra A.M. Maggioni C. Sitia R. 2000. Degradation of unassembled soluble Ig subunits by cytosolic proteasomes: evidence that retrotranslocation and degradation are coupled events. FASEB J. 14 (5): 769-778. 10744633.
20. Meunier L. Usherwood Y.K. Chung K.T. Hendershot L.M. 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell, 13 (12): 4456-4469. 10.1091/mbc.E02-05-0311. 12475965.
21. Mezghrani A. Fassio A. Benham A. Simmen T. Braakman I. Sitia R. 2001. Manipulation of oxidative protein folding and PDI redox state in mammalian cells. EMBO J. 20 (22): 6288-6296. 10.1093/emboj/20.22.6288. 11707400.
22. Molinari M. Helenius A. 1999. Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature, 402 (6757): 90-93. 10.1038/47062. 10573423.
23. Molinari M. Galli C. Piccaluga V. Pieren M. Paganetti P. 2002. Sequential assistance of molecular chaperones and transient formation of covalent complexes during protein degradation from the ER. J. Cell Biol. 158 (2): 247-257. 10.1083/jcb.200204122. 12119363.
24. Moore P. Bernardi K.M. Tsai B. 2010. The Ero1alpha-PDI redox cycle regulates retro-translocation of cholera toxin. Mol. Biol. Cell, 21 (7): 1305-1313. 10.1091/mbc.E09-09-0826. 20130085.
25. Pagani M. Fabbri M. Benedetti C. Fassio A. Pilati S. Bulleid N.J. et al 2000. Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 275 (31): 23685-23692. 10.1074/jbc.M003061200. 10818100.
26. Römisch K. 1999. Surfing the Sec61 channel: bidirectional protein translocation across the ER membrane. J. Cell Sci. 112 (23): 4185-4191. 10564637.
27. Schelhaas M. Malmström J. Pelkmans L. Haugstetter J. Ellgaard L. Grünewald K. Helenius A. 2007. Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell, 131 (3): 516-529. 10.1016/j.cell.2007.09.038. 17981119.
28. Sitia R. Braakman I. 2003. Quality control in the endoplasmic reticulum protein factory. Nature, 426 (6968): 891-894. 10.1038/nature02262. 14685249.
29. Tortorella D. Story C.M. Huppa J.B. Wiertz E.J. Jones T.R. Bacik I. et al 1998. Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J. Cell Biol. 142 (2): 365-376. 10.1083/jcb.142.2.365. 9679137.
30. Tsai B. Rapoport T.A. 2002. Unfolded cholera toxin is transferred to the ER membrane and released from protein disulfide isomerase upon oxidation by Ero1. J. Cell Biol. 159 (2): 207-216. 10.1083/jcb.200207120. 12403808.
31. Tsai B. Rodighiero C. Lencer W.I. Rapoport T.A. 2001. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell, 104 (6): 937-948. 10.1016/S0092-8674(01)00289-6. 11290330.
32. Vembar S.S. Brodsky J.L. 2008. One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9 (12): 944-957. 10.1038/nrm2546. 19002207.
33. Walczak C.P. Bernardi K.M. Tsai B. 2012. Endoplasmic reticulum-dependent redox reactions control endoplasmic reticulum-associated degradation and pathogen entry. Antioxid. Redox Signal. 16 (8): 809-818. 10.1089/ars.2011.4425. 22142231.