Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: Importance of oligosaccharide processing, ubiquitination, and proteasome-dependent removal from ER membranes

Journal of Experimental Medicine

Volumn 187, Issue 6, 1998, Pages 835-846

  Yang, Mei ^a   Omura, Satoshi ^b   Bonifacino, Juan S ^c   Weissman, Allan M ^a,d  

^a NATIONAL CANCER INSTITUTE   (United States)

^b KITASATO INSTITUTE   (Japan)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; MANNOSIDASE; OLIGOSACCHARIDE; PROTEASOME; RECEPTOR SUBUNIT; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; MEMBRANE BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE RECEPTOR GENE;

ANIMALS; ANTIGENS, CD3; CYSTEINE ENDOPEPTIDASES; ENDOPLASMIC RETICULUM; MANNOSIDASES; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MULTIENZYME COMPLEXES; OLIGOSACCHARIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; UBIQUITINS;

EID: 0032536903     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.6.835     Document Type: Article

References (55)

1. Weissman, A.M. 1994. The T-cell antigen receptor: a multisubunit signaling complex. Chem. Immunol. 59:1-18.
2. Sussman, J.J., J.S. Bonifacino, J. Lippincott-Schwartz, A.M. Weissman, T. Saito, R.D. Klausner, and J.D. Ashwell. 1988. Failure to synthesize the T cell CD3-ζ chain: structure and function of a partial T cell receptor complex. Cell. 52:85-95.
3. Klausner, R.D., J. Lippincott-Schwartz, and J.S. Bonifacino. 1990. The T cell antigen receptor: insights into organelle biology. Annu. Rev. Cell. Biol. 6:403-431.
4. Bonifacino, J.S., and J. Lippincott-Schwartz. 1991. Degradation of proteins within the endoplasmic reticulum. Curr. Opin. Cell. Biol. 3:592-600.
5. + thymocytes influenced by CD4. Nature. 344:247-251.
6. Kearse, K.P., J.L. Roberts, T.I. Munitz, D.L. Wiest, T. Nakayama, and A. Singer. 1994. Developmental regulation of αβ T cell antigen receptor expression results from differential stability of nascent TCR-α proteins within the endoplasmic reticulum of immature and mature T cells. EMBO (Eur. Mol. Biol. Organ.) J. 13:4504-4514.
7. Bonifacino, J.S., C.K. Suzuki, J. Lippincott-Schwartz, A.M. Weissman, and R.D. Klausner. 1989. Pre-Golgi degradation of newly synthesized T cell antigen receptor chains: intrinsic sensitivity and the role of subunit assembly. J. Cell. Biol. 109: 73-83.
8. Bonifacino, J.S., C.K. Suzuki, and R.D. Klausner. 1990. A peptide sequence confers retention and degradation in the endoplasmic reticulum. Science. 247:79-82.
9. Shin, J., S. Lee, and J.L. Strominger. 1993. Translocation of TCRα chains into the lumen of the endoplasmic reticulum and their degradation. Science. 259:1901-1904.
10. Coux, O., K. Tanaka, and A.L. Goldberg. 1996. Structure and function or the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:801-847.
11. Weissman, A.M. 1997. Regulating protein degradation by ubiquitination. Immunol. Today. 18:189-198.
12. Biederer, T., C. Volkwein, and T. Sommer. 1996. Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway. EMBO (Eur. Mol. Biol. Organ.) J. 15:2069-2076.
13. Hiller, M.M., A. Finger, M. Schweiger, and D.H. Wolf. 1996. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science. 273:1725-1728.
14. Werner, E.D., J.L. Brodsky, and A.A. McCracken. 1996. Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc. Natl. Acad. Sci. USA. 93:13797-13801.
15. Ward, C.L., S. Ōmura, and R.R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell. 83: 121-127.
16. Jensen, T.J., M.A. Loo, S. Pind, D.B. Williams, A.L. Goldberg, and J.R. Riordan. 1995. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell. 83:129-135.
17. Qu, D., J.H. Teckman, S. Ōmura, and D.H. Perlmutter. 1990. Degradation of a mutant secretory protein, α1-antitrypsin Z, in the endoplasmic reticulum requires proteasome activity. J. Biol. Chem. 271:22791-22795.
18. McGee, T.P., H.H. Cheng, H. Kumagai, S. Ōmura, and R.D. Simoni. 1996. Degradation of 3-hydroxy-3-methylglutaryl-CoA reductase in endoplasmic reticulum membranes is accelerated as a result of increased susceptibility to proteolysis. J. Biol. Chem. 271:25630-25638.
19. Wiertz, E.J., T.R. Jones, L. Sun, M. Bogyo, H.J. Geuze, and H.L. Ploegh. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell. 84:769-779.
20. Wiertz, E.J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T.R. Jones, T.A. Rapoport, and H.L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature. 384: 432-438.
21. Hughes, E.A., C. Hammond, and P. Cresswell. 1997. Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. USA. 94:1896-1901.
22. Lord, M.J. 1996. Protein degradation: go outside and see the proteasome. Curr. Biol. 6:1067-1069.
23. Bonifacino, J.S. 1996. Reversal of fortune for nascent proteins. Nature. 384:405-406.
24. Kopito, R.H. 1997. ER quality control: the cytoplasmic connection. Cell. 88:427-430.
25. van den Elsen, P., B.-A. Shepley, M. Cho, and C. Terhorst. 1985. Isolation and characterization of a cDNA clone encoding the murine homolgue of the human 20K T3/T-cell receptor glycoprotein. Nature. 314:542-544.
26. Sussman, J.J., T. Saito, E.M. Shevach, R.N. Germain, and J.D. Ashwell. 1988. Thy-1- and Ly-6-mediated lymphokine production and growth inhibition of a T cell hybridoma require co-expression of the T cell antigen receptor complex. J. Immunol. 140:2520-2526.
27. Hyman, R., and V. Stallings. 1974. Complementary patterns of Thy-1 variants and evidence that antigen loss variants "pre-exist" in the parental population. J. Natl. Cancer Inst. 52: 429-437.
28. Yang, M., J. Ellenberg, J.S. Bonifacino, and A.M. Weissman. 1997. The transmembrane domain of a carboxyl-terminal anchored protein determines localization to the endoplasmic reticulum. J. Biol. Chem. 272:1970-1975.
29. Samelson, L.E., A.M. Weissman, F.A. Robey, I. Berkower. and R.D. Klausner. 1986. Characterization of an anti-peptide antibody that recognizes the murine analogue of the human T cell antigen receptor-T3 δ chain. J. Immunol. 137:3254-3258.
30. Cenciarelli, C., K.J. Wilhelm, Jr., A. Guo, and A.M. Weissman. 1996. T cell antigen receptor ubiquitination is a consequence of receptor-mediated tyrosine kinase activation. J. Biol. Chem. 271:8709-8713.
31. Leo, O., M. Foo, D.H. Sachs, L.E. Samelson, and J.A. Bluestone. 1987. Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc. Natl. Acad. Sci. USA. 84: 1374-1378.
32. Kubo, R.T., W. Born, J.W. Kappler, P. Marrack, and M. Pigeon. 1989. Characterization of a monoclonal antibody which detects all murine αβ T cell receptors. J. Immunol. 142:2736-2742.
33. Chen, C., J.S. Bonifacino, L.C. Yuan, and R.D. Klausner. 1988. Selective degradation of T cell antigen receptor chains retained in a pre-Golgi compartment. J. Cell Biol. 107:2149-2161.
34. Cenciarelli, C., D. Hou, K.-C. Hsu, B.L. Rellahan, D.L. Wiest, H.T. Smith, V.A. Fried, and A.M. Weissman. 1992. Activation-induced ubiquitination of the T cell antigen receptor. Science. 257:795-797.
35. Rock, K.L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A.L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 78:761-771.
36. Chen, Z., J. Hagler, V.J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Gen. Dev. 9:1586-1597.
37. Fenteany, G., R.F. Standaert, G.A. Reichard, E.J. Corey, and S.L. Schreiber. 1994. A β-lactone related to lactacystin induces neurite outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc. Natl. Acad. Sci. USA. 91:3358-3362.
38. Hedrick, S.M., L.A. Matis, T.T. Hecht, L.E. Samelson, D.L. Longo, E. Heber Katz, and R.H. Schwartz. 1982. The fine specificity of antigen and Ia determinant recognition by T cell hybridoma clones specific for pigeon cytochrome c. Cell. 30:141-152.
39. Elbein, A.D. 1991. Glycosidase inhibitors: inhibitors of N-linked oligosaccharide processing. FASEB (Fed. Am. Soc. Exp. Biol.) J. 5:3055-3063.
40. Ashwell, J.D., and A.M. Weissman. 1995. T Cell Antigen Receptor Genes, Gene Products and Co-receptors. R.R. Rich, T.A. Fleisher, B.D. Schwartz, W.T. Shearer, and W. Strober, editors. Mosby-Year Book, Inc., St. Louis, MO. 69-93.
41. Chien, Y., D.M. Becker, T. Lindsten, M. Okamura, D.I. Cohen, and M.M. Davis. 1984. A third type of murine T-cell receptor gene. Nature. 312:31-35.
42. Huppa, J.B., and H.L. Ploegh. 1997. The α chain of the T cell antigen receptor is degraded in the cytosol. Immunity. 7:113-122.
43. Yu, H., G. Kaung, S. Kobayashi, and R.R. Kopito. 1997. Cytosolic degradation of T-cell receptor α chains by the proteasome. J. Biol. Chem. 272:20800-20804.
44. Lippincott-Schwartz, J., J.S. Bonifacino, L.C. Yuan, and R.D. Klausner. 1988. Degradation from the endoplasmic reticulum: disposing of newly synthesized proteins. Cell. 54: 209-220.
45. Kearse, K.P., D.B. Williams, and A. Singer. 1994. Persistence of glucose residues on core oligosaccharides prevents association of TCR-α and TCR-β proteins with calnexin and results specifically in accelerated degradation of nascent TCR-α proteins within the endoplasmic reticulum. EMBO (Eur. Mol. Biol. Organ.) J. 13:3678-3686.
46. Plemper, R.K., S. Bohmler, J. Bordallo, T. Sommer, and D.H. Wolf. 1997. Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature. 388:891-895.
47. Hammond, C., and A. Helenius. 1995. Quality control in the secretory pathway. Curr. Opin. Cell. Biol. 7:523-529.
48. Su, K., T. Stoller, J. Rocco, J. Zemsky, and R. Green. 1993. Pre-Golgi degradation of yeast prepro-α-factor expressed in a mammalian cell. J. Biol. Chem. 268:14301-14309.
49. Liu, Y., P. Choudhury, C.M. Cabral, and R.N. Sifers. 1997. Intracellular disposal of incompletely folded human α1-antitrypsin involves release from calnexin and post-translational trimming of asparagine-linked oligosaccharides. J. Biol. Chem. 272:7946-7951.
50. van Leeuwen, J.E.M., and K.P. Kearse. 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.
51. van Leeuwen, J.E.M., and K.P. Kearse. 1996. Calnexin associates exclusively with individual CD3 delta 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.
52. Palmer, A., A.J. Rivett, S. Thomson, K.B. Hendil, G.W. Butcher, G. Fuertes, and E. Knecht. 1996. Subpopulations of proteasomes in rat liver nuclei, microsomes and cytosol. Biochem. J. 316:401-407.
53. Rivett, A.J., A. Palmer, and E. Knecht. 1992. Electron microscopic localization of the multicatalytic proteinase complex in rat liver and in cultured cells. J. Histochem. Cytochem. 40:1165-1172.
54. Yang, Y., K. Fruh, K. Ahn, and P.A. Peterson. 1995. In vivo assembly of the proteasomal complexes, implications for antigen processing. J. Biol. Chem. 270:27687-27694.
55. Sommer, T., and S. Jentsch. 1993. A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature. 365:176-179.