Cooperation of ER-60 and BiP in the oxidative refolding of denatured proteins in vitro

Journal of Biochemistry

Volumn 138, Issue 6, 2005, Pages 773-780

  Okudo, Hirokazu ^a   Kato, Hiroyuki ^a   Arakaki, Yukino ^a   Urade, Reiko ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

BiP; ER 60; Molecular chaperone; Protein folding; Thiol disulfide oxidoreductase

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALPHA LACTALBUMIN; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; IOXAGLIC ACID; RIBONUCLEASE;

ARTICLE; DENATURATION; IN VITRO STUDY; PROTEIN FOLDING; REACTION ANALYSIS; SURFACE PLASMON RESONANCE;

HEAT-SHOCK PROTEINS; HUMANS; LACTALBUMIN; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; PROTEIN RENATURATION; RIBONUCLEASES; SURFACE PLASMON RESONANCE;

EID: 32944458162     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvi166     Document Type: Article

References (44)

1. Noiva, R. and Lennarz, W.J. (1992) Protein disulfide isomerase. A multifunctional protein resident in the lumen of the endoplasmic reticulum. J. Biol. Chem. 267, 3553-3556
2. Freedman, R.B., Hirst, T.R., and Tuite, M.F. (1994) Protein disulfide isomerase: building bridges in protein folding. Trends Biochem. Sci. 19, 331-336
3. Gilbert, H.F. (1998) Protein disulfide isomerase. In Methods in Enzymology (Lorimer, G.H. and Baldwin, T.O., eds.) Vol. 290, pp. 26-50, Academic Press, New York
4. Puig, A. and Gilbert, H.F. (1994) Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. J. Biol. Chem. 269, 7764-7771
5. Whiteley, E.M., Hsu, T.-A., and Betenbaugh, M.J. (1997) Thioredoxin domain non-equivalence and anti-chaperone activity of protein disulfide isomerase mutants in vivo. J. Biol. Chem. 272, 22556-22563
6. Chandrashekar, R., Tsuji, N., Morales, T., Ozols, V., and Mehta, K. (1998) An ERp60-like protein from the filarial parasite Dirofilaria immitis has both transglutaminase and protein disulfide isomerase activity. Proc. Natl. Acad. Sci. USA 95, 531-536
7. Wetterau, J.R., Combs, K.A., Spinner, S.N., and Joiner, B.J. (1990) Protein disulfide isomerase is a component of the microsomal triglyceride transfer protein complex. J. Biol. Chem. 265, 9800-9807
8. Wetterau, J.R., Combs, K.A., McLean, L.R., Spinner, S.N., and Aggerbeck, L.P. (1991) Protein disulfide isomerase appears necessary to maintain the catalytically active structure of the microsomal triglyceride transfer protein. Biochemistry 30, 9728-9735
9. Pihlajaniemi, T., Helaakoski, T., Tasanen, K., Myllylä, R., Huhtala, M.-L., Koivu, J., and Kivirikko, K.I. (1987) Molecular cloning of the β-subunit of human prolyl 4-hydroxylase. This subunit and protein disulfide isomerase are products of the same gene. EMBO J. 6, 643-649
10. Tasanen, K., Parkkonen, T., Chow, L.K., Kivirikko, K.I., and Pihlajaniemi, T. (1988) Characterization of the human gene for a polypeptide that acts both as the β subunit of prolyl 4-hydroxylase and as protein disulfide isomerase. J. Biol. Chem. 263, 16218-16224
11. Bourdi, M., Demady, D., Martin, J.L., Jabbour, S.K., Martin, B.M., George, J.W., and Pohl, L.R. (1995) cDNA cloning and baculovirus expression of the human liver endoplasmic reticulum P58: characterization as a protein disulfide isomerase isoform, but not as a protease or a carnitine acyltransferase. Arch. Biochem. Biophys. 323, 397-403
12. Urade, R., Nasu, M., Moriyama, T., Wada, K., and Kito, M. (1992) Protein degradation by the phosphoinositide-specific phospholipase C-alpha family from rat liver endoplasmic reticulum. J. Biol. Chem. 267, 15152-15159
13. Urade, R. and Kito, M. (1992) Inhibition by acidic phospholipids of protein degradation by ER-60 protease, a novel cysteine protease, of endoplasmic reticulum. FEBS Lett. 312, 83-86
14. Urade, R., Oda, T., Ito, H., Moriyama, T., Utsumi, S., and Kito, M. (1997) Functions of characteristic Cys-Gly-His-Cys (CGHC) and Gln-Glu-Asp-Leu (QEDL) motifs of microsomal ER-60 protease. J. Biochem. 122, 834-842
15. Okudo, H., Kito, M., Moriyama, T., Ogawa, T., and Urade, R. (2002) Transglutaminase activity of human ER-60. Biosci. Biotechnol. Biochem. 66, 1423-1426
16. Zapun, A., Darby, N.J., Tessier, D.C., Michalak, M., Bergeron, J.J.M., and Thomas, D.Y. (1998) Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J. Biol. Chem. 273, 6009-6012
17. Urade, R., Okudo, H., Kato, H., Moriyama, T., and Arakaki, Y. (2004) ER-60 domains responsible for interaction with calnexin and calreticulin. Biochemistry 43, 8858-8868
18. Klappa, P., Ruddock, L.W., Darby, N.J., and Freedman, R.B. (1998) 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
19. Elliott, J.G., Oliver, J.D., and High, S. (1997) The thiol-dependent reductase ERp57 interacts specifically with N-glycosylated integral membrane proteins. J. Biol. Chem. 272, 13849-13855
20. Oliver, J.D., van der Wal, F.J., Bulleid, N.J., and High, S. (1997) Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins, Science 275, 86-88
21. Molinari, M. and Helenius, A. (1999) Glycoproteins form mixed disulfides with oxidoreductases during folding in living cells. Nature 402, 90-93
22. Silvennoinen, L., Myllyharju, J., Ruoppolo, M., Orrù, S., Caterino, M., Kivirikko, K.I., and Koivunen, P. (2004) Identification and characterization of structural domains of human ERp57: association with calreticulin requires several domains. J. Biol. Chem. 14, 13607-13615
23. Russell, S., Ruddock, L.W., Salo, K.E.H., Oliver, J.D., Poebuck, Q.P., Llewellyn, D.H., Roderick, H.L., Koivunen, P., Myllyharju, J., and High, S. (2004) The primary substrate binding site in the b′ domain of ERp57 is adapted for endoplasmic reticulum lectin association. J. Biol. Chem. 279, 18861-18869
24. Pollpck, S., Kozlov, G., Pelletier, M.-F., Trempe, J.-F., Jansen, G., Sitnikov, D., Bergeron, J.J., Gehring, K., Ekiel, I., and Thomas, D.Y. (2004) Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. EMBO J. 23, 1020-1029
25. Frickel, E., Riek, R., Jelesarov, I., Helenius, A., Wüthrich, K., and Ellgaard, L. (2001) TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. USA 99, 1954-1959
26. Leach, M.R., Cohen-Doyle, M.F., Thomas, D.Y., and Williams, D.B. (2002) Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J. Biol. Chem. 277, 29686-29697
27. Meunier, L., Usherwood, Y.-K., Chung, T., and Hendershot, L.M. (2002) A subset of chaperones and folding enzymes from multiprotein complexes in endoplasmic reticulum to bind proteins. Mol. Biol. Cell 13, 4456-4469
28. Mayer, M., Kies, U., Kammermeier, R., and Buchner, J. (2000) BiP and PDI cooperate in the oxidative folding of antibodies in vitro. J. Biol. Chem. 275, 29421-29425
29. Mayer, M., Frey, S., Koivunen, P., Myllyharju, J., and Buchner, J. (2004) Influence of the oxidoreductase ERp57 on the folding of an antibody Fab fragment. J. Mol. Biol. 341, 1077-1084
30. McCormick, L.M., Urade, R., Arakaki, Y., Schwartz, A.L., and Bu, G. (2005) Independent and cooperative roles of N-glycans and molecular chaperones in the folding and disulfide bond formation of the low-density lipoprotein (LDL) receptor-related protein. Biochemistry 44, 5794-5803
31. Adeli, K., Macri, J., Mohammadi, A., Kito, M., Urade, R., and Cavallo, D. (1997) Apolipoprotein B is intracellularly associated with an ER-60 protease homologue in HepG2 cells. J. Biol. Chem. 272, 22489-22494
32. Reisfeld, R.A., Lewis, D.E., and Williams, D.E. (1962) Disk electrophoresis of basic proteins and peptides on polyacrylamide gels. Nature 195, 281-283
33. Ewbank, J.J. and Creighton, T.E. (1993) Pathway of disulfide-coupled unfolding and refolding of bovine alfa-lactalbumin. Biochemistry 32, 3677-3693
34. Davis, B.J. (1964) Disc electrophoresis. II. Method application to human serum proteins. Ann. N.Y. Acad. Sci. 121, 404-427
35. Seals, J.R., McDonald, J.M., Bruns, D., and Jarett, L. (1978) A sensitive and precise isotopic assay of ATPase activity. Anal. Biochem. 90, 785-795
36. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
37. Blond-Elguindi, S., Fourie, A.M., Sambrook, J.F., and Gething, M.-J.H. (1993) Peptide-dependent stimulation of the ATPase activity of the molecular chaperone BiP is the result of conversion of oligomers to active monomers. J. Biol. Chem. 268, 12730-12735
38. Flynn, G.C., Pohl, J., Flocco, M.T., and Rothman, J.E. (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature 353, 726-731
39. Blond-Elguindi, S., Cwirla, S.E., Dower, W.J., Lipshutz, R.J., Sprang, S.R., Sambrook, J.F., and Gething, M.-J.H. (1993) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75, 717-728
40. Wang, T., Chang, J., and Wang, C. (1993) Identification of the peptide binding domain of hsc70. 18-Kilodalton fragment located immediately after ATPase domain is sufficient for high affinity binding. J. Biol. Chem. 268, 26049-26051
41. Morshauser, R.C., Wang, H., Flynn, G.C., and Zuiderweg, E.R.P. (1995) The peptide-binding domain of the chaperone protein Hsc70 has an unusual secondary structure topology. Biochemistry 34, 6261-6266
42. Wei, J., Gaut, J.R., and Hendershot, L.M. (1995) In vitro dissociation of BiP-peptide complexes requires a conformational change in BiP after ATP binding but does not require ATP hydrolysis. J. Biol. Chem. 270, 26677-26682
43. Kuznetsov, G., Chen, L.B., and Nigam, S.K. (1997) Multiple molecular chaperones complex with misfolded large oligomeric glycoproteins in the endoplasmic reticulum. J. Biol. Chem. 272, 3057-3063
44. Kimura, T., Imaishi, K., Hagiwara, Y., Horibe, T., Hayano, T., Takahashi, N., Urade, R., Kato K., and Kikuchi, M. (2005) ERp57 binds competitively to protein disulfide isomerase and calreticulin. Biochem. Biophys. Res. Commun. 331, 224-230