Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules

doi:10.1083/jcb.112.6.1099

This Article

	Full Text (PDF, 3288K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Degen, E.
	Articles by Williams, D. B.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Degen, E.
	Articles by Williams, D. B.


Social Bookmarking

	What's this?

ARTICLES

Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules

E Degen and DB Williams
Department of Biochemistry, University of Toronto, Canada.

Chemical cross-linking and gel permeation chromatography were used to examine early events in the biogenesis of class I histocompatibility molecules. We show that newly synthesized class I heavy chains associate rapidly and quantitatively with an 88-kD protein in three murine tumor cell lines. This protein (p88) does not appear to possess Asn-linked glycans and it is not the abundant ER protein, GRP94. The class I-p88 complex exists transiently (t1/2 = 20-45 min depending on the specific class I heavy chain) and several lines of evidence suggest that p88 dissociates from the complex while still in the ER. Dissociation is not triggered upon binding of beta 2-microglobulin to the heavy chain (t1/2 = 2-5 min). However, the rate of dissociation does correlate with the characteristic rate of ER to Golgi transport for the particular class I molecule studied. Consequently, dissociation of p88 may be rate limiting for ER to Golgi transport. Class I molecules bind antigenic peptides, apparently in the ER, for subsequent presentation to cytotoxic T lymphocytes at the cell surface. p88 could promote peptide binding or it may retain class I molecules in the ER during formation of the ternary complex of heavy chain, beta 2- microglobulin, and peptide.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Tourdot, S., Nejmeddine, M., Powis, S. J., Gould, K. G. (2005). Different MHC Class I Heavy Chains Compete with Each Other for Folding Independently of {beta}2-Microglobulin and Peptide. J. Immunol. 174: 925-933 [Abstract] [Full Text]
Mizrachi, D., Segaloff, D. L. (2004). Intracellularly Located Misfolded Glycoprotein Hormone Receptors Associate with Different Chaperone Proteins than Their Cognate Wild-Type Receptors. Mol. Endocrinol. 18: 1768-1777 [Abstract] [Full Text]
Boisrame, A., Chasles, M., Babour, A., Beckerich, J.-M., Gaillardin, C. (2003). Sbh1p, a subunit of the Sec61 translocon, interacts with the chaperone calnexin in the yeast Yarrowia lipolytica. J. Cell Sci. 115: 4947-4956 [Abstract] [Full Text]
Schell, T. D., Mylin, L. M., Tevethia, S. S., Joyce, S. (2002). The assembly of functional {beta}2-microglobulin-free MHC class I molecules that interact with peptides and CD8+ T lymphocytes. Int Immunol 14: 775-782 [Abstract] [Full Text]
Yu, Y. Y. L., Harris, M. R., Lybarger, L., Kimpler, L. A., Myers, N. B., Virgin IV, H. W., Hansen, T. H. (2002). Physical Association of the K3 Protein of Gamma-2 Herpesvirus 68 with Major Histocompatibility Complex Class I Molecules with Impaired Peptide and {beta}2-Microglobulin Assembly. J. Virol. 76: 2796-2803 [Abstract] [Full Text]
Tan, P., Kropshofer, H., Mandelboim, O., Bulbuc, N., Hammerling, G. J., Momburg, F. (2002). Recruitment of MHC Class I Molecules by Tapasin into the Transporter Associated with Antigen Processing-Associated Complex Is Essential for Optimal Peptide Loading. J. Immunol. 168: 1950-1960 [Abstract] [Full Text]
De Silva, A. D., Park, J.-J., Matsuki, N., Stanic, A. K., Brutkiewicz, R. R., Medof, M. E., Joyce, S. (2002). Lipid Protein Interactions: The Assembly of CD1d1 with Cellular Phospholipids Occurs in the Endoplasmic Reticulum. J. Immunol. 168: 723-733 [Abstract] [Full Text]
Su, R.-C., Miller, R. G. (2001). Stability of Surface H-2Kb, H-2Db, and Peptide-Receptive H-2Kb on Splenocytes. J. Immunol. 167: 4869-4877 [Abstract] [Full Text]
Paulsson, K. M., Wang, P., Anderson, P. O., Chen, S., Pettersson, R. F., Li, S. (2001). Distinct differences in association of MHC class I with endoplasmic reticulum proteins in wild-type, and {beta}2-microglobulin- and TAP-deficient cell lines. Int Immunol 13: 1063-1073 [Abstract] [Full Text]
Harris, M. R., Lybarger, L., Yu, Y. Y. L., Myers, N. B., Hansen, T. H. (2001). Association of ERp57 with Mouse MHC Class I Molecules Is Tapasin Dependent and Mimics That of Calreticulin and not Calnexin. J. Immunol. 166: 6686-6692 [Abstract] [Full Text]
Ritz, U., Momburg, F., Pircher, H.-P., Strand, D., Huber, C., Seliger, B. (2001). Identification of sequences in the human peptide transporter subunit TAP1 required for transporter associated with antigen processing (TAP) function. Int Immunol 13: 31-41 [Abstract] [Full Text]
Myers, N. B., Harris, M. R., Connolly, J. M., Lybarger, L., Yu, Y. Y. L., Hansen, T. H. (2000). Kb, Kd, and Ld Molecules Share Common Tapasin Dependencies as Determined Using a Novel Epitope Tag. J. Immunol. 165: 5656-5663 [Abstract] [Full Text]
Ho, S. C., Chaudhuri, S., Bachhawat, A., McDonald, K., Pillai, S. (2000). Accelerated Proteasomal Degradation of Membrane Ig Heavy Chains. J. Immunol. 164: 4713-4719 [Abstract] [Full Text]
Danilczyk, U. G., Cohen-Doyle, M. F., Williams, D. B. (2000). Functional Relationship between Calreticulin, Calnexin, and the Endoplasmic Reticulum Luminal Domain of Calnexin. J. Biol. Chem. 275: 13089-13097 [Abstract] [Full Text]
Fu, J., Kreibich, G. (2000). Retention of Subunits of the Oligosaccharyltransferase Complex in the Endoplasmic Reticulum. J. Biol. Chem. 275: 3984-3990 [Abstract] [Full Text]
Yu, Y. Y. L., Myers, N. B., Hilbert, C. M., Harris, M. R., Balendiran, G. K., Hansen, T. H. (1999). Definition and transfer of a serological epitope specific for peptide-empty forms of MHC class I. Int Immunol 11: 1897-1906 [Abstract] [Full Text]
De Silva, A. D., Boesteanu, A., Song, R., Nagy, N., Harhaj, E., Harding, C. V., Joyce, S. (1999). Thermolabile H-2Kb Molecules Expressed by Transporter Associated with Antigen Processing-Deficient RMA-S Cells Are Occupied by Low-Affinity Peptides. J. Immunol. 163: 4413-4420 [Abstract] [Full Text]
Chiu, N. M., Chun, T., Fay, M., Mandal, M., Wang, C.-R. (1999). The Majority of H2-M3 Is Retained Intracellularly in a Peptide-Receptive State and Traffics to the Cell Surface in the Presence of N-Formylated Peptides. JEM 190: 423-434 [Abstract] [Full Text]
Zheng, P., Sarma, S., Guo, Y., Liu, Y. (1999). Two Mechanisms for Tumor Evasion of Preexisting Cytotoxic T-Cell Responses: Lessons from Recurrent Tumors. Cancer Res. 59: 3461-3467 [Abstract] [Full Text]
Suh, W.-K., Derby, M. A., Cohen-Doyle, M. F., Schoenhals, G. J., Fruh, K., Berzofsky, J. A., Williams, D. B. (1999). Interaction of Murine MHC Class I Molecules with Tapasin and TAP Enhances Peptide Loading and Involves the Heavy Chain {alpha}3 Domain. J. Immunol. 162: 1530-1540 [Abstract] [Full Text]
Gao, Y.-s., Alvarez, C., Nelson, D. S., Sztul, E. (1998). Molecular Cloning, Characterization, and Dynamics of Rat Formiminotransferase Cyclodeaminase, a Golgi-associated 58-kDa Protein. J. Biol. Chem. 273: 33825-33834 [Abstract] [Full Text]
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]
Linnik, K. M., Herscovitz, H. (1998). Multiple Molecular Chaperones Interact with Apolipoprotein B during Its Maturation. THE NETWORK OF ENDOPLASMIC RETICULUM-RESIDENT CHAPERONES (ERp72, GRP94, CALRETICULIN, AND BiP) INTERACTS WITH APOLIPOPROTEIN B REGARDLESS OF ITS LIPIDATION STATE. J. Biol. Chem. 273: 21368-21373 [Abstract] [Full Text]
Choi, E. Y., Park, W. S., Jung, K. C., Kim, S. H., Kim, Y. Y., Lee, W. J., Park, S. H. (1998). Engagement of CD99 Induces Up-Regulation of TCR and MHC Class I and II Molecules on the Surface of Human Thymocytes. J. Immunol. 161: 749-754 [Abstract] [Full Text]
Harris, M. R., Yu, Y. Y. L., Kindle, C. S., Hansen, T. H., Solheim, J. C. (1998). Calreticulin and Calnexin Interact with Different Protein and Glycan Determinants During the Assembly of MHC Class I. J. Immunol. 160: 5404-5409 [Abstract] [Full Text]
de Virgilio, M., Weninger, H., Ivessa, N. E. (1998). Ubiquitination Is Required for the Retro-translocation of a Short-lived Luminal Endoplasmic Reticulum Glycoprotein to the Cytosol for Degradation by the Proteasome. J. Biol. Chem. 273: 9734-9743 [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]
Gabathuler, R., Alimonti, J., Zhang, Q.-J., Kolaitis, G., Reid, G., Jefferies, W. A. (1998). Surrogate Antigen Processing Mediated by TAP-dependent Antigenic Peptide Secretion. JCB 140: 17-27 [Abstract] [Full Text]
Mosse, C. A., Meadows, L., Luckey, C. J., Kittlesen, D. J., Huczko, E. L., Slingluff, C. L. Jr., Shabanowitz, J., Hunt, D. F., Engelhard, V. H. (1998). The Class I Antigen-processing Pathway for the Membrane Protein Tyrosinase Involves Translation in the Endoplasmic Reticulum and Processing in the Cytosol. JEM 187: 37-48 [Abstract] [Full Text]
Li, X., Su, R. T. C., Hsu, H.-t., Sze, H. (1998). The Molecular Chaperone Calnexin Associates with the Vacuolar H+-ATPase from Oat Seedlings. Plant Cell 10: 119-130 [Abstract] [Full Text]
Machold, R. P., Ploegh, H. L. (1996). Intermediates in the Assembly and Degradation of Class I Major Histocompatibility Complex (MHC) Molecules Probed with Free Heavy Chain-specific Monoclonal Antibodies. JEM 184: 2251-2260 [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]
Van Leeuwen, J. E.M., Kearse, K. P. (1996). The Related Molecular Chaperones Calnexin and Calreticulin Differentially Associate with Nascent T Cell Antigen Receptor Proteins within the Endoplasmic Reticulum. J. Biol. Chem. 271: 25345-25349 [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]
Oliver, J. D., Hresko, R. C., Mueckler, M., High, S. (1996). The Glut 1Glucose Transporter Interacts with Calnexin and Calreticulin. J. Biol. Chem. 271: 13691-13696 [Abstract] [Full Text]
van Leeuwen, J. E. M., Kearse, K. P. (1996). Calnexin Associates Exclusively with Individual CD3[IMAGE] and T Cell Antigen Receptor (TCR) alpha Proteins Containing Incompletely Trimmed Glycans That Are Not Assembled into Multisubunit TCR Complexes. J. Biol. Chem. 271: 9660-9665 [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]
Wada, I., Imai, S.-i., Kai, M., Sakane, F., Kanoh, H. (1995). Chaperone Function of Calreticulin When Expressed in the Endoplasmic Reticulum as the Membrane-anchored and Soluble Forms. J. Biol. Chem. 270: 20298-20304 [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]
Otsu, M., Urade, R., Kito, M., Omura, F., Kikuchi, M. (1995). A Possible Role of ER-60 Protease in the Degradation of Misfolded Proteins in the Endoplasmic Reticulum. J. Biol. Chem. 270: 14958-14961 [Abstract] [Full Text]
Gelman, M. S., Chang, W., Thomas, D. Y., Bergeron, J. J. M., Prives, J. M. (1995). Role of the Endoplasmic Reticulum Chaperone Calnexin in Subunit Folding and Assembly of Nicotinic Acetylcholine Receptors. J. Biol. Chem. 270: 15085-15092 [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]
Nauseef, W. M., McCormick, S. J., Clark, R. A. (1995). Calreticulin Functions as a Molecular Chaperone in the Biosynthesis of Myeloperoxidase. J. Biol. Chem. 270: 4741-4747 [Abstract] [Full Text]
Jannatipour, M., Rokeach, L. A. (1995). The Schizosaccharomyces pombe Homologue of the Chaperone Calnexin Is Essential for Viability. J. Biol. Chem. 270: 4845-4853 [Abstract] [Full Text]
Arunachalam, B., Cresswell, P. (1995). Molecular Requirements for the Interaction of Class II Major Histocompatibility Complex Molecules and Invariant Chain with Calnexin. J. Biol. Chem. 270: 2784-2790 [Abstract] [Full Text]
Cotner, T., Pious, D. (1995). HLA-DRbeta Chains Enter into an Aggregated Complex Containing GRP-78/BiP Prior to Their Degradation by the Pre-Golgi Degradative Pathway. J. Biol. Chem. 270: 2379-2386 [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.R., Fruh, K., Karlsson, L., Teyton, L., Yang, Y., Peterson, P.A. (1995). Assembly and Intracellular Transport of MHC Class I and Class II Molecules. Cold Spring Harb Symp Quant Biol 60: 249-261 [Abstract]
Hebert, D.N., Simons, J.F., Peterson, J.R., Helenius, A. (1995). Calnexin, Calreticulin, and Bip/Kar2p in Protein Folding. Cold Spring Harb Symp Quant Biol 60: 405-415 [Abstract]
Hammond, C, Helenius, A (1994). Folding of VSV G protein: sequential interaction with BiP and calnexin. Science 266: 456-458 [Abstract]
Suh, W., Cohen-Doyle, M., Fruh, K, Wang, K, Peterson, P., Williams, D. (1994). Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 264: 1322-1326 [Abstract]
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]
Agard, D. (1993). To fold or not to fold.... Science 260: 1903-1904
Fahnestock, M., Tamir, I, Narhi, L, Bjorkman, P. (1992). Thermal stability comparison of purified empty and peptide-filled forms of a class I MHC molecule. Science 258: 1658-1662 [Abstract]
Click, E.-M., Anderson, K.S., Androlewicz, M.J., Wei, M.L., Cresswell, P. (1992). Transport and Expression of Class I MHC Glycoproteins in an Antigen-processing Mutant Cell Line. Cold Spring Harb Symp Quant Biol 57: 571-577 [Abstract]
Dettenhofer, M., Yu, X.-F. (2001). Characterization of the Biosynthesis of Human Immunodeficiency Virus Type 1 Env from Infected T-cells and the Effects of Glucose Trimming of Env on Virion Infectivity. J. Biol. Chem. 276: 5985-5991 [Abstract] [Full Text]