Efficient dissociation of the p88 chaperone from major histocompatibility complex class I molecules requires both beta 2- microglobulin and peptide

doi:10.1084/jem.175.6.1653

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Efficient dissociation of the p88 chaperone from major histocompatibility complex class I molecules requires both beta 2- microglobulin and peptide

E Degen, MF Cohen-Doyle and DB Williams
Department of Biochemistry, University of Toronto, Ontario, Canada.

Previously, we showed that an 88-kD protein (p88) associates rapidly and quantitatively with newly synthesized murine major histocompatibility complex class I molecules within the endoplasmic reticulum (ER). This interaction is transient and dissociation of p88 appears to be rate limiting for transport of class I molecules from the ER to the Golgi apparatus. In this report, we examine the relationship between p88 interaction and assembly of the ternary complex of class I heavy chain beta 2-microglobulin (beta 2m), and peptide ligand. In both murine and human beta 2m-deficient cells, in which little or no transport of class I heavy chains is observed, p88 remained associated with intracellular heavy chains throughout their lifetime. In murine RMA-S cells, which are apparently defective in accumulating peptide ligands for class I within the ER, prolonged association of p88 with "empty" heavy chain-beta 2m heterodimers was also observed. However, p88 dissociated slowly in parallel with the slow rate of ER to Golgi transport of empty class I molecules in these cells. The close correlation between p88 association and impaired class I transport suggests that p88 functions to retain incompletely assembled class I molecules in the ER. We propose that conformational changes in class I heavy chains induced by the binding of both beta 2m and peptide are required for efficient p88 dissociation and subsequent class I transport.
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Deng, Y., Gibbs, J., Bacik, I., Porgador, A., Copeman, J., Lehner, P., Ortmann, B., Cresswell, P., Bennink, J. R., Yewdell, J. W. (1998). Assembly of MHC Class I Molecules with Biosynthesized Endoplasmic Reticulum-Targeted Peptides Is Inefficient in Insect Cells and Can Be Enhanced by Protease Inhibitors. J. Immunol. 161: 1677-1685 [Abstract] [Full Text]
Robinson, P. J., Travers, P. J., Stackpoole, A., Flaherty, L., Djaballah, H. (1998). Maturation of Qa-1b Class I Molecules Requires {beta}2-Microglobulin But Is TAP Independent. J. Immunol. 160: 3217-3224 [Abstract] [Full Text]
Zhang, Q., Salter, R. D. (1998). Distinct Patterns of Folding and Interactions with Calnexin and Calreticulin in Human Class I MHC Proteins with Altered N-Glycosylation. J. Immunol. 160: 831-837 [Abstract] [Full Text]
Wolpert, E. Z., Petersson, M., Chambers, B. J., Sandberg, J. K., Kiessling, R., Ljunggren, H.-G., Karre, K. (1997). Generation of CD8+ T cells specific for transporter associated with antigen processing deficient�cells. Proc. Natl. Acad. Sci. USA 94: 11496-11501 [Abstract] [Full Text]
Day, P. M., Yewdell, J. W., Porgador, A., Germain, R. N., Bennink, J. R. (1997). Direct delivery of exogenous MHC class I molecule-binding oligopeptides to the endoplasmic reticulum of viable�cells. Proc. Natl. Acad. Sci. USA 94: 8064-8069 [Abstract] [Full Text]
Van�Leeuwen, J.�E.�M., Kearse, K.�P. (1996). Deglucosylation of N-linked glycans is an important step in the dissociation of calreticulin-class I-TAP�complexes. Proc. Natl. Acad. Sci. USA 93: 13997-14001 [Abstract] [Full Text]
Shtrom, S. S., Hall, Z. W. (1996). Formation of a Ligand-binding Site for the Acetylcholine Receptor in Vitro. J. Biol. Chem. 271: 25506-25514 [Abstract] [Full Text]
Balow, J. P., Weissman, J. D., Kearse, K. P. (1995). Unique Expression of Major Histocompatibility Complex Class I Proteins in the Absence of Glucose Trimming and Calnexin Association. J. Biol. Chem. 270: 29025-29029 [Abstract] [Full Text]
Tector, M., Salter, R. D. (1995). Calnexin Influences Folding of Human Class I Histocompatibility Proteins but Not Their Assembly with beta(2)-Microglobulin. J. Biol. Chem. 270: 19638-19642 [Abstract] [Full Text]
Ware, F. E., Vassilakos, A., Peterson, P. A., Jackson, M. R., Lehrman, M. A., Williams, D. B. (1995). The Molecular Chaperone Calnexin Binds Glc(1)Man(9)GlcNAc(2) Oligosaccharide as an Initial Step in Recognizing Unfolded Glycoproteins. J. Biol. Chem. 270: 4697-4704 [Abstract] [Full Text]
Zhang, Q., Tector, M., Salter, R. D. (1995). Calnexin Recognizes Carbohydrate and Protein Determinants of Class I Major Histocompatibility Complex Molecules. J. Biol. Chem. 270: 3944-3948 [Abstract] [Full Text]
Sugita, M., Brenner, M. B. (1995). Association of the Invariant Chain with Major Histocompatibility Complex Class I Molecules Directs Trafficking to Endocytic Compartments. J. Biol. Chem. 270: 1443-1448 [Abstract] [Full Text]
Parlati, F., Dominguez, M., Bergeron, J. J. M., Thomas, D. Y. (1995). Saccharomyces cerevisiae CNE1 Encodes an Endoplasmic Reticulum (ER) Membrane Protein with Sequence Similarity to Calnexin and Calreticulin and Functions as a Constituent of the ER Quality Control Apparatus. J. Biol. Chem. 270: 244-253 [Abstract] [Full Text]
Jackson, M., Cohen-Doyle, M., Peterson, P., Williams, D. (1994). Regulation of MHC class I transport by the molecular chaperone, calnexin (p88, IP90). Science 263: 384-387 [Abstract]
Rajagopalan, S, Xu, Y, Brenner, M. (1994). Retention of unassembled components of integral membrane proteins by calnexin. Science 263: 387-390 [Abstract]