Removal and degradation of the free MHC class II β chain in the endoplasmic reticulum requires proteasomes and is accelerated by BFA

Journal of Cell Science

Volumn 111, Issue 15, 1998, Pages 2217-2226

  Dusseljee, Simone ^a   Wubbolts, Richard ^a   Verwoerd, Desiree ^a   Tulp, Abraham ^a   Janssen, Hans ^a   Calafat, Jero ^a   Neefjes, Jacques ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Antigen presentation; Brefeldin A; ER degradation; MHC class II molecule; Proteasome

Indexed keywords

BREFELDIN A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEASOME;

ARTICLE; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ACETYLCYSTEINE; ANTI-BACTERIAL AGENTS; BREFELDIN A; CELL FRACTIONATION; CELL LINE; CYCLOPENTANES; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-B27 ANTIGEN; HUMANS; KIDNEY; MACROLIDES; MULTIENZYME COMPLEXES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SYNTHESIS INHIBITORS; RECOMBINANT FUSION PROTEINS;

EID: 0031665311     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Amitay, R., Shachar, I., Rabinovich, E., Haimovich, J. and Bar-Nun, S. (1992). Degradation of secretory immunoglobulin M in B lymphocytes occurs in a post-endoplasmic reticulum compartment and is mediated by a cystein protease. J. Biol. Chem. 267, 20694-20700.
2. Biederer, T., Volkwein, C. and Sommer, T. (1996). Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway. EMBO J. 15, 2069-2076.
3. Biederer, T., Volkwein, C. and Sommer, T. (1997) Role of Cue1p in ubiqitination and degradation at the ER surface. Science 278, 1806-1809.
4. Bogyo, M., McMaster, J. S., Gaczynska, M., Tortorella, IX, Goldberg, A. L. and Ploegh, H. (1997). Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HsIV by a new class of inhibitors. Proc. Nat. Acad. Sci. USA 94, 6629-6634.
5. Bonifacino, J. S., Suzuki, C. K. and Klausner, R. D. (1990). A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum. Science 247, 79-82.
6. Bonifacino, J. S. (1996). Reversal of fortune for nascent proteins. Nature 384, 405-406.
7. Brown, J. H., Jardetzky, T. S., Golga, J. C., Stem, L. J., Urban, R. G. Strominger, J. L. and Wiley, D. C. (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364, 33-39.
8. Chen, C., Bonifacino, J. S., Yuan, L. C. and Klausner, R. D. (1988) Selective degradation of T cell antigen receptor chains retained in a pre-Golgi compartment. J. Cell Biol. 107, 2149-2161.
9. Cotner, T. and Pious, D. (1995). HLA-DR beta 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.
10. Dick, L. R., Cruikshank, A. A., Grenier, L., Melandri, F. D., Nunes, S. L. and Stein, R. L. (1996). Mechanistic studies on the inactivation of the proteasome by lactacystin. J. Biol. Chem. 271, 7273-7276.
11. Fenteany, G., Standaert, R. F., Lane, W. S., Choi, S., Corey, E. J. and Schreiber, S. L. (1995). Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268, 726-731.
12. Finger, A., Knop, M. and Wolf, D. H. (1993). Analysis of two mutated vacuolar proteins reveals a degradation pathway in the endoplasmic reticulum or a related compartment of yeast. Eur. J. Biochim. 218, 565-574.
13. Flynn, G. C., Pohl, J., Flocco, M. T. and Rothman, J. E. (1991). Peptide-binding specificity of the molecular chaperone BiP. Nature 353, 726-730.
14. Hamman, B. D., Hendershot, L. M. and Johnson, A. E. (1998). BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92, 725-734
15. Hammond, C., Braakman, I. and Helenius, A. (1994). Role of N-linked oligosaccharide recognition, glucose trimming and calnexin in glycoprotein folding and quality control. Proc. Nat. Acad. Sci. USA 91, 913-917.
16. Hiller, M. M., Finger, A., Schweiger, M. and Wolf, D. H. (1996) ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 273, 1725-1728.
17. Hochstenbach, F., David, V., Watkins, S. and Brenner, M. B. (1992) Endoplasmic reticulum resident protein of 90 kilodaltons associates with the T- and B-cell antigen receptors and major histocompatibility complex antigens during their assembly. Proc. Nat. Acad. Sci. USA 89, 4734-4738.
18. Hsu, V. W., Yuan, L. C., Nuchtern, J. G., Lippincott-Schwartz, J., Hämmerling, G. J. and Klausner, R. D. (1991). A recycling pathway between the endoplasmic reticulum and the Golgi apparatus for retention of unassembled MHC class I molecules. Nature 352, 441-444.
19. Huppa, J. B. and Ploegh, H. L. (1997). The alpha chain of the T cell antigen receptor is degraded in the cytosol. Immunity 7, 113-122.
20. Hurtley, S. M. and Helenius, A. (1989) Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 277-307.
21. Jensen, T. J., Loo, M. A., Pind, S., Williams, D. B., Goldberg, A. L. and Riordan, J. R. (1995). Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135.
22. Kearse, K. P., Williams, D. B. and Singer, A. (1994). Persistence of glucose residues on core oligosaccharides prevents association of TCRα and TCRβ proteins with calnexin and results specifically in accelerated degradation of nascent TCRα proteins within the endoplasmic reticulum. EMBO J. 13, 3678-3686.
23. Klausner, R. D. and Sitia, R. (1990). Protein degradation in the endoplasmic reticulum. Cell 62, 611-614.
24. Koppelman, B. and Cresswell, P. (1990) Rapid nonlysosomal degradation of assembled HLA class II glycoproteins incorporating a mutant DR alpha-chain. J. Immunol. 145, 2730-2736.
25. Lippincott-Schwartz, J., Bonifacino, J. S., Yuan, L. C. and Klausner, R. D. (1988). Degradation from the endoplasmic reticulum: disposing of newly synthesized proteins. Cell 54, 209-220.
26. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S. and Klausner, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
27. McCracken, A. A. and Brodsky, J. L. (1996). Assembly of ER-associated protein degradation in vitro: dependence on cytosol. calnexin and ATP. J. Cell Biol. 32, 291-298.
28. Neefjes, J. J., Stollorz, V., Peters, P. J., Geuze, H. J. and Ploegh, H. L. (1990). The biosynthetic pathway of MHC class II but not MHC class I molecules intersects the endocytic route. Cell 61, 171-183.
29. Nijenhuis, M., Calafat, J., Kuijpers, K. C., Janssen, H., de Haas, M., Nodeng, T. W., Bakke, O. and Neefjes, J. J. (1994). Targeting major histocompatibility complex class II molecules to the cell surface by invariant chain allows antigen presentation upon recycling Eur. J. Immunol. 24, 873-883.
30. Nijenhuis, M. and Neefjes, J. J. (1994). Early events in the assembly of major histocompatibilily complex class II heterotrimers from their free subunits. Eur. J. Immunol. 24, 247-256.
31. Otsu, M., Urade, R., Kito, M., Omura, F. and 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.
32. Palmer, A., Rivett, A. J., Thomson, S., Hendil, K. B., Butcher, G. W., Fuertes, G. and Knecht, E. (1996). Subpopulations of proteasomes in rat liver nuclei, microsomes and cytosol. Biochem. J. 316, 401-407.
33. Pilon, M., Schekman, R. and Romisch, K. (1997). Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J. 16, 4540-4548.
34. Plemper, R. K., Bohmler, S., Bordallo, J., Sommer, T. and Wolf, D. H. (1997). Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature 388, 891-895.
35. Raposo, G., VanSanten, H. M., Leijendekker, R., Geuze, H. J. and Ploegh, H. L. (1995). Misfolded major histocompatibility complex class I molecules accumulate in an expanded ER-Golgi intermediate compartment. J. Cell Biol. 131, 1403-1419.
36. Reits, E. A. J., Benham, A. M., Plougastel, B., Neefjes, J. and Trowsdale, J. (1997) Dynamics of proteasome distribution in living cells. EMRO J. 16, 6087-6094.
37. Schweitzer, A., Matter, K., Ketcham, C. M. and Hauri, H.-P. (1991). The isolated ER-Golgi intermediate compartment exhibits properties that are different from ER and cis-Golgi. J. Cell Biol. 113, 45-54.
38. Shaw, S., Ziegler, A. and DeMars, R. (1985). Specificity of monoclonal antibodies directed against human and murine class II histocompatibility antigens as analyzed by binding to HLA-deletion mutant cell lines. Human Immunol. 12, 191-211.
39. Sommer, T. and Jentsch, S. (1993). A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature 365, 176-179.
40. Stafford, K. J. and Bonifacino, J. S. (1991). A permeabilized cell system identities the endoplasmic reticulum as a site of protein degradation. J. Cell Biol. 115, 1225-1236.
41. Stam, N. J., Spits, H. and Ploegh, H. L. (1986). Monoclonal antibodies raised against denatured HLA-B locus H-chains permit biochemical characterization of certain HLA-C locus products. J. Immunol. 37, 2299-2306.
42. Tulp, A., Verwoerd, D., Fernandez-Borja, M., Neefjes, J. and Hart, A. A. M. (1996). High resolution density gradient electrophoresis of cellular organelles. Electrophoresis 17, 173-178.
43. Ward, C. L., Omura, S. and Kopito, R. R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
44. Wikström, L. and Lodish, F. (1991). Unfolded H2b asialoglycoprotein receptor subunit polypeptides are selectively degraded within the endoplasmic reticulum. J. Cell Biol. 113, 997-1007.
45. Wiertz, K. J., Jones, T. R., Sun, L., Bogyo, M., Geuze, H. J. and Ploegh, H. L. (1996a). The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779.
46. Wiertz, E. J. H. J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T. A. and Ploegh, H. L. (1996b). Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.
47. Wileman, T., Kane, L. P., Young, J., Carson, G. R. and Terhorst, C. (1993) Association between subunit ectodomains promote T cell antigen receptor assembly and protect against degradation in the ER. J. Cell Biol. 122, 67-78.
48. Wubbolts, R., Fernandez-Borja, M., Oomen, L., Verwoerd, D., Janssen, H., Calafat, J., Tulp, A., Dusseljee, S. and Neefjes, J. (1996). Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135, 611-622.
49. Yang, M., Omura, S., Bonifacino, J. S. and Weissman, A. M. (1998). Novel aspects of degradation of T cell receptor subunits form the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing. ubiquitination, and proteasome-dependent removal from ER membranes. J. Exp. Med. 187, 835-846.
50. Yang, Y., Fruh, K., Ahn, K. and Peterson, P. A. (1995). In vivo assembly of the proteasomal complexes, implications for antigen processing. J. Biol. Chem. 270, 27687-27694.