Retrotranslocation of MHC class I heavy chain from the endoplasmic reticulum to the cytosol is dependent on ATP supply to the ER lumen

Molecular Immunology

Volumn 40, Issue 10, 2004, Pages 733-741

  Albring, Jörn ^a   Koopmann, Jens Oliver ^a,b   Hämmerling, Günter J ^a   Momburg, Frank ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b The Switchback   (United Kingdom)

Author keywords

ATP; Chaperones; Endoplasmic reticulum; MHC class I heavy chain; Retrotranslocation

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTEASOME;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENERGY METABOLISM; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HYDROLYSIS; MEMBRANE TRANSPORT; MICROSOME; MINOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY;

EID: 0344413468     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2003.08.008     Document Type: Article

References (44)

1. Antoniou A.N., Ford S., Alphey M., Osborne A., Elliott T., Powis S.J. The oxidoreductase ERp57 efficiently reduces partially folded in preference to fully folded MHC class I molecules. EMBO J. 21:2002;2655-2663.
2. Bacik I., Snyder H.L., Anton L.C., Russ G., Chen W., Bennink J.R., Urge L., Otvos L., Dudkowska B., Eisenlohr L., Yewdell J.W. Introduction of a glycosylation site into a secreted protein provides evidence for an alternative antigen processing pathway: transport of precursors of major histocompatibility complex class I-restricted peptides from the endoplasmic reticulum to the cytosol. J. Exp. Med. 186:1997;479-487.
3. 2-microglobulin antibody and its use in the genetic and biochemical analysis of major histocompatibility antigens. Eur. J. Immunol. 9:1979;536-545.
4. Brodsky J.L., Werner E.D., Dubas M.E., Goeckeler J.L., Kruse K.B., McCracken A.A. The requirement for molecular chaperones during endoplasmic reticulum-associated protein degradation demonstrates that protein export and import are mechanistically distinct. J. Biol. Chem. 274:1999;3453-3460.
5. Brooks P., Fuertes G., Murray R.Z., Bose S., Knecht E., Rechsteiner M.C., Hendil K.B., Tanaka K., Dyson J., Rivett J. Subcellular localization of proteasomes and their regulatory complexes in mammalian cells. Biochem J. 346:2000;155-161.
6. Chillarón J., Haas I.G. Dissociation from BiP and retrotranslocation of unassembled immunoglobulin light chains are tightly coupled to proteasome activity. Mol. Biol. Cell. 11:2000;217-226.
7. Cresswell P., Bangia N., Dick T., Diedrich G. The nature of the MHC class I peptide loading complex. Immunol. Rev. 172:1999;21-28.
8. DeMartino G.N., Slaughter C.A. The proteasome, a novel protease regulated by multiple mechanisms. J. Biol. Chem. 274:1999;22123-22126.
9. Farmery M.R., Allen S., Allen A.J., Bulleid N.J. The role of ERp57 in disulfide bond formation during the assembly of major histocompatibility complex class I in a synchronized semipermeabilized cell translation system. J. Biol. Chem. 275:2000;14933-14938.
10. Gillece P., Luz J.M., Lennarz W.J., de la Cruz F.J., Römisch K. Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J. Cell Biol. 147:1999;1443-1456.
11. Gillece P., Pilon M., Römisch K. The protein translocation channel mediates glycopeptide export across the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 97:2000;4609-4614.
12. Hughes E.A., Cresswell P. The thiol oxidoreductase ERp57 is a component of the MHC class I peptide-loading complex. Curr. Biol. 8:1998;709-712.
13. Hughes E.A., Hammond C., Cresswell P. Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. U.S.A. 94:1997;1896-1901.
14. Huppa J.B., Ploegh H.L. The α chain of the T cell antigen receptor is degraded in the cytosol. Immunity. 7:1997;113-122.
15. Jarosch E., Taxis C., Volkwein C., Bordallo J., Finley D., Wolf D.H., Sommer T. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4:2002;134-139.
16. Kaltoft M.B., Koch C., Uerkvitz W., Hendil K.B. Monoclonal antibodies to the human multicatalytic proteinase (proteasome). Hybridoma. 11:1992;507-517.
17. Kikkert M., Hassink G., Barel M., Hirsch C., van der Wal F.J., Wiertz E. Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of MHC class I molecules from the endoplasmic reticulum to the cytosol. Biochem J. 358:2001;369-377.
18. Koopmann J.O., Albring J., Hüter E., Bulbuc N., Spee P., Neefjes J., Hämmerling G.J., Momburg F. Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity. 13:2000;117-127.
19. Lindquist J.A., Jensen O.N., Mann M., Hämmerling G.J. ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J. 17:1998;2186-2195.
20. Mayer T.U., Braun T., Jentsch S. Role of the proteasome in membrane extraction of a short-lived ER-transmembrane protein. EMBO J. 17:1998;3251-3257.
21. Mayinger P., Meyer D.I. An ATP transporter is required for protein translocation into the yeast endoplasmic reticulum. EMBO J. 12:1993;659-666.
22. Momburg F., Tan P. Tapasin - the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol. Immunol. 39:2002;217-233.
23. Momburg F., Ortiz-Navarrete V., Neefjes J., Goulmy E., van de Wal Y., Spits H., Powis S.J., Butcher G.W., Howard J.C., Walden P., Hämmerling G.J. Proteasome subunits encoded by the major histocompatibility complex are not essential for antigen presentation. Nature. 360:1992;174-177.
24. Mosse C.A., Meadows L., Luckey C.J., Kittlesen D.J., Huczko E.L., Slingluff C.L., Shabanowitz J., Hunt D.F., Engelhard V.H. The class I antigen-processing pathway for the membrane protein tyrosinase involves translation in the endoplasmic reticulum and processing in the cytosol. J. Exp. Med. 187:1998;37-48.
25. 2+. J. Biol. Chem. 270:1995;18051-18059.
26. Plemper R.K., Böhmler S., Bordallo J., Sommer T., Wolf D.H. Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature. 388:1997;891-895.
27. Plemper R.K., Egner R., Kuchler K., Wolf D.H. Endoplasmic reticulum degradation of a mutated ATP-binding cassette transporter Pdr5 proceeds in a concerted action of Sec61 and the proteasome. J. Biol. Chem. 273:1998;32848-32856.
28. Römisch K. Surfing the Sec61 channel: bidirectional protein translocation across the ER membrane. J. Cell Sci. 112:1999;4185-4191.
29. Rouiller I., Butel V.M., Latterich M., Milligan R.A., Wilson-Kubalek E.M. A major conformational change in p97 AAA ATPase upon ATP binding. Mol. Cell. 6:2000;1485-1490.
30. Schubert U., Antón L.C., Bacik I., Cox J.H., Bour S., Bennink J.R., Orlowski M., Strebel K., Yewdell J.W. CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J. Virol. 72:1998;2280-2288.
31. Shamu C.E., Story C.M., Rapoport T.A., Ploegh H.L. The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate. J. Cell Biol. 147:1999;45-58.
32. Shamu C.E., Flierman D., Ploegh H.L., Rapoport T.A., Chau V. Polyubiquitination is required for US11-dependent movement of MHC class I heavy chain from endoplasmic reticulum into cytosol. Mol. Biol. Cell. 12:2001;2546-2555.
33. Stam N.J., Spits H., Ploegh H.L. Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J. Immunol. 137:1986;2299-2306.
34. Tortorella D., Story C.M., Huppa J.B., Wiertz E.J., Jones T.R., Bacik I., Bennink J.R., Yewdell J.W., Ploegh H.L. Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J. Cell. Biol. 142:1998;365-376.
35. Tsai B., Ye Y., Rapoport T.A. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell Biol. 3:2002;246-255.
36. Walter P., Blobel G. Preparation of microsomal membranes for cotranslational protein translocation. Methods Enzymol. 96:1983;84-93.
37. Wang Q., Chang A. Eps1, a novel PDI-related protein involved in ER quality control in yeast. EMBO J. 18:1999;5972-5982.
38. Wei J., Gaut J.R., Hendershot L.M. 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. 270:1995;26677-26682.
39. Wiertz E.J., Jones T.R., Sun L., Bogyo M., Geuze H.J., Ploegh H.L. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell. 84:1996a;769-779.
40. Wiertz E.J., Tortorella D., Bogyo M., Yu J., Mothes W., Jones T.R., Rapoport T.A., Ploegh H.L. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature. 384:1996;432-438.
41. Wilkinson K.D. Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin. Cell Dev. Biol. 11:2000;141-148.
42. Wilson C.M., Farmery M.R., Bulleid N.J. Pivotal role of calnexin and mannose trimming in regulating the endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain. J. Biol. Chem. 275:2000;21224-21232.
43. Yang Y., Früh K., Ahn K., Peterson P.A. In vivo assembly of the proteasomal complexes, implications for antigen processing. J. Biol. Chem. 270:1995;27687-27694.
44. Ye Y., Meyer H.H., Rapoport T.A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature. 414:2001;652-656.