DOI: 10.1083/jcb.147.1.45. The Pathway of Us11-Dependent Degradation of Mhc Class I Heavy Chains Involves a Ubiquitin-Conjugated Intermediate

The Pathway of Us11-Dependent Degradation of Mhc Class I Heavy Chains Involves a Ubiquitin-Conjugated Intermediate

10.1083/jcb.147.1.45

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The human cytomegalovirus protein, US11, initiates the destruction of MHC class I heavy chains by targeting them for dislocation from the ER to the cytosol and subsequent degradation by the proteasome. We report the development of a permeabilized cell system that recapitulates US11-dependent degradation of class I heavy chains. We have used this system, in combination with experiments in intact cells, to identify and order intermediates in the US11-dependent degradation pathway. We find that heavy chains are ubiquitinated before they are degraded. Ubiquitination of the cytosolic tail of heavy chain is not required for its dislocation and degradation, suggesting that ubiquitination occurs after at least part of the heavy chain has been dislocated from the ER. Thus, ubiquitination of the heavy chain does not appear to be the signal to start dislocation. Ubiquitinated heavy chains are associated with membrane fractions, suggesting that ubiquitination occurs while the heavy chain is still bound to the ER membrane. Our results support a model in which US11 co-opts the quality control process by which the cell destroys misfolded ER proteins in order to specifically degrade MHC class I heavy chains.

Bibliography

Shamu, C. E., Story, C. M., Rapoport, T. A., & Ploegh, H. L. (1999). The Pathway of Us11-Dependent Degradation of Mhc Class I Heavy Chains Involves a Ubiquitin-Conjugated Intermediate. The Journal of Cell Biology, 147(1), 45â58.

Authors 4

Caroline E. Shamu (first)
Craig M. Story (additional)
Tom A. Rapoport (additional)
Hidde L. Ploegh (additional)

References 42 Referenced 132

10.1073/pnas.93.20.10990 / Proc. Natl. Acad. Sci. USA. / Human cytomegalovirus inhibits antigen presentation by a sequential multistep process by Ahn (1996)
10.1074/jbc.271.5.2823 / J. Biol. Chem. / Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5 by Baboshina (1996)
10.1016/0003-9861(85)90046-3 / Arch. Biochem. Biophys. / Characterization of protein transport between successive compartments of the Golgi apparatusasymmetric properties of donor and acceptor activities in a cell-free system by Balch (1985)
10.1016/S0021-9258(18)53371-8 / J. Biol. Chem. / The bacterially expressed yeast CDC34 gene product can undergo autoubiquitination to form a multiubiquitin chain-linked protein by Banerjee (1993)
10.1002/j.1460-2075.1996.tb00560.x / EMBO (Eur. Mol. Biol. Organ.) J. / Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway by Biederer (1996)
10.1126/science.278.5344.1806 / Science / Role of Cue1p in ubiquitination and degradation at the ER surface by Biederer (1997)
10.1073/pnas.94.13.6629 / Proc. Natl. Acad. Sci. USA. / Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors by Bogyo (1997)
10.1073/pnas.77.3.1365 / Proc. Natl. Acad. Sci. USA. / ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation by Ciechanover (1980)
10.1074/jbc.273.16.9734 / J. Biol. Chem. / Ubiquitination is required for the retro-translocation of a short-lived luminal endoplasmic reticulum glycoprotein to the cytosol for degradation by the proteasome by deVirgilio (1998)
10.1016/S0092-8674(00)80404-3 / Cell / A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p by Feldman (1997)
10.1111/j.1432-1033.1993.tb18410.x / Eur. J. Biochem. / Analysis of two mutated vacuolar proteins reveals a degradation pathway in the endoplasmic reticulum or a related compartment of yeast by Finger (1993)
10.1016/0092-8674(93)90483-7 / Cell / Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane by Gorlich (1993)
10.1016/S0021-9258(17)38895-6 / J. Biol. Chem. / The immunochemical detection and quantitation of intracellular ubiquitin-protein conjugates by Haas (1985)
10.1073/pnas.94.24.12944 / Proc. Natl. Acad. Sci. USA. / Ubiquitin-mediated regulation of 3-hydroxy-3-methylglutaryl-CoA reductase by Hampton (1997)
{'key': '2023072900595578400_HarlowandLane1988', 'volume-title': 'AntibodiesA Laboratory Manual', 'author': 'Harlow', 'year': '1988'} / AntibodiesA Laboratory Manual by Harlow (1988)
10.1126/science.273.5282.1725 / Science / ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway by Hiller (1996)
10.1073/pnas.94.5.1896 / Proc. Natl. Acad. Sci. USA. / Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome by Hughes (1997)
10.1016/S1074-7613(00)80514-2 / Immunity / The alpha chain of the T cell antigen receptor is degraded in the cytosol by Huppa (1997)
10.1083/jcb.143.7.1883 / J. Cell Biol. / Aggresomesa cellular response to misfolded proteins by Johnston (1998)
10.1128/jvi.69.8.4830-4841.1995 / J. Virol. / Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains by Jones (1995)
10.1016/S0092-8674(00)81881-4 / Cell / ER quality controlthe cytoplasmic connection by Kopito (1997)
10.1093/emboj/17.12.3251 / EMBO (Eur. Mol. Biol. Organ.) J. / Role of the proteasome in membrane extraction of a short-lived ER-transmembrane protein by Mayer (1998)
10.1083/jcb.132.3.291 / J. Cell Biol. / Assembly of ER-associated protein degradation in vitrodependence on cytosol, calnexin, and ATP by McCracken (1996)
10.1007/BF00373817 / Immunogenetics / An analysis of class I antigens of man and other species by one-dimensional IEF and immunoblotting by Neefjes (1986)
10.1093/emboj/16.15.4540 / EMBO (Eur. Mol. Biol. Organ.) J. / Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation by Pilon (1997)
10.1038/42276 / Nature / Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation by Plemper (1997)
{'key': '2023072900595578400_Ploegh1995', 'first-page': '10', 'article-title': 'One-dimensional isoelectric focusing of proteins in slab gels', 'volume-title': 'Current Protocols in Protein Science', 'author': 'Ploegh', 'year': '1995'} / Current Protocols in Protein Science / One-dimensional isoelectric focusing of proteins in slab gels by Ploegh (1995)
10.1074/jbc.271.37.22791 / J. Biol. Chem. / Degradation of a mutant secretory protein, alpha1-antitrypsin Z, in the endoplasmic reticulum requires proteasome activity by Qu (1996)
10.1016/S0952-7915(98)80040-X / Curr. Opin. Immunol. / Intracellular distribution of proteasomes by Rivett (1998)
10.1038/365176a0 / Nature / A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum by Sommer (1993)
10.1096/fasebj.11.14.9409541 / FASEB J. / Endoplasmic reticulum degradationreverse protein flow of no return by Sommer (1997)
10.1073/pnas.96.15.8516 / Proc. Natl. Acad. Sci. USA. / The cytosolic tail of class I MHC heavy chain is required for its dislocation by the human cytomegalovirus US2 and US11 gene products by Story (1999)
{'key': '2023072900595578400_SurdejandJacobs-Lorena1994', 'first-page': '560', 'article-title': 'Strategy for epitope tagging the protein-coding region of any gene', 'volume': '17', 'author': 'Surdej', 'year': '1994', 'journal-title': 'Biotechniques.'} / Biotechniques. / Strategy for epitope tagging the protein-coding region of any gene by Surdej (1994)
10.1016/S0021-9258(17)32485-7 / J. Biol. Chem. / Purification and enzymatic properties of peptide:N-glycanase from C3H mouse-derived L-929 fibroblast cells. Possible widespread occurrence of post-translational remodification of proteins by N-deglycosylation by Suzuki (1994)
10.1083/jcb.116.6.1357 / J. Cell Biol. / Retrograde transport from the Golgi region to the endoplasmic reticulum is sensitive to GTP gamma S by Tan (1992)
10.1083/jcb.142.2.365 / J. Cell Biol. / Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential by Tortorella (1998)
10.1159/000131967 / Cytogenet. Cell Genet. / Localization of a gene controlling the expression of the human transferrin receptor to the region q12 leads to qter of chromosome 3 by van de Rijn (1983)
10.1016/0092-8674(95)90240-6 / Cell / Degradation of CFTR by the ubiquitin-proteasome pathway by Ward (1995)
10.1016/S0092-8674(00)81054-5 / Cell / The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol by Wiertz (1996)
10.1038/384432a0 / Nature / Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction by Wiertz (1996)
10.1074/jbc.272.33.20800 / J. Biol. Chem. / Cytosolic degradation of T-cell receptor alpha chains by the proteasome by Yu (1997)
10.1083/jcb.123.6.1735 / J. Cell Biol. / Two pathways for the degradation of the H2 subunit of the asialoglycoprotein receptor in the endoplasmic reticulum by Yuk (1993)

Dates

Type	When
Created	23 years ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years ago (July 28, 2023, 9 p.m.)
Indexed	4 months ago (April 23, 2025, 9:14 p.m.)
Issued	25 years, 10 months ago (Oct. 4, 1999)
Published	25 years, 10 months ago (Oct. 4, 1999)
Published Online	25 years, 10 months ago (Oct. 4, 1999)
Published Print	25 years, 10 months ago (Oct. 4, 1999)

Funders 0

None

BibTeX

@article{Shamu_1999, title={The Pathway of Us11-Dependent Degradation of Mhc Class I Heavy Chains Involves a Ubiquitin-Conjugated Intermediate}, volume={147}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.147.1.45}, DOI={10.1083/jcb.147.1.45}, number={1}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Shamu, Caroline E. and Story, Craig M. and Rapoport, Tom A. and Ploegh, Hidde L.}, year={1999}, month=oct, pages={45–58} }

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      "first-page": "10990",
      "DOI": "10.1073/pnas.93.20.10990",
      "article-title": "Human cytomegalovirus inhibits antigen presentation by a sequential multistep process",
      "volume": "93",
      "author": "Ahn",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900595578400_BaboshinaandHaas1996",
      "doi-asserted-by": "crossref",
      "first-page": "2823",
      "DOI": "10.1074/jbc.271.5.2823",
      "article-title": "Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5",
      "volume": "271",
      "author": "Baboshina",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072900595578400_BalchandRothman1985",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1016/0003-9861(85)90046-3",
      "article-title": "Characterization of protein transport between successive compartments of the Golgi apparatusasymmetric properties of donor and acceptor activities in a cell-free system",
      "volume": "240",
      "author": "Balch",
      "year": "1985",
      "journal-title": "Arch. Biochem. Biophys."
    },
    {
      "key": "2023072900595578400_Banerjeeetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "5668",
      "DOI": "10.1016/S0021-9258(18)53371-8",
      "article-title": "The bacterially expressed yeast CDC34 gene product can undergo autoubiquitination to form a multiubiquitin chain-linked protein",
      "volume": "268",
      "author": "Banerjee",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072900595578400_Biedereretal1996",
      "doi-asserted-by": "crossref",
      "first-page": "2069",
      "DOI": "10.1002/j.1460-2075.1996.tb00560.x",
      "article-title": "Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway",
      "volume": "15",
      "author": "Biederer",
      "year": "1996",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900595578400_Biedereretal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1806",
      "DOI": "10.1126/science.278.5344.1806",
      "article-title": "Role of Cue1p in ubiquitination and degradation at the ER surface",
      "volume": "278",
      "author": "Biederer",
      "year": "1997",
      "journal-title": "Science"
    },
    {
      "key": "2023072900595578400_Bogyoetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "6629",
      "DOI": "10.1073/pnas.94.13.6629",
      "article-title": "Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors",
      "volume": "94",
      "author": "Bogyo",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900595578400_Ciechanoveretal1980",
      "doi-asserted-by": "crossref",
      "first-page": "1365",
      "DOI": "10.1073/pnas.77.3.1365",
      "article-title": "ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation",
      "volume": "77",
      "author": "Ciechanover",
      "year": "1980",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900595578400_deVirgilioetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "9734",
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      "volume": "273",
      "author": "deVirgilio",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
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      "first-page": "221",
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      "article-title": "A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p",
      "volume": "91",
      "author": "Feldman",
      "year": "1997",
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    {
      "key": "2023072900595578400_Fingeretal1993",
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      "first-page": "565",
      "DOI": "10.1111/j.1432-1033.1993.tb18410.x",
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      "volume": "218",
      "author": "Finger",
      "year": "1993",
      "journal-title": "Eur. J. Biochem."
    },
    {
      "key": "2023072900595578400_GorlichandRapoport1993",
      "doi-asserted-by": "crossref",
      "first-page": "615",
      "DOI": "10.1016/0092-8674(93)90483-7",
      "article-title": "Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane",
      "volume": "75",
      "author": "Gorlich",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2023072900595578400_HaasandBright1985",
      "doi-asserted-by": "crossref",
      "first-page": "12464",
      "DOI": "10.1016/S0021-9258(17)38895-6",
      "article-title": "The immunochemical detection and quantitation of intracellular ubiquitin-protein conjugates",
      "volume": "260",
      "author": "Haas",
      "year": "1985",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072900595578400_HamptonandBhakta1997",
      "doi-asserted-by": "crossref",
      "first-page": "12944",
      "DOI": "10.1073/pnas.94.24.12944",
      "article-title": "Ubiquitin-mediated regulation of 3-hydroxy-3-methylglutaryl-CoA reductase",
      "volume": "94",
      "author": "Hampton",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900595578400_HarlowandLane1988",
      "volume-title": "AntibodiesA Laboratory Manual",
      "author": "Harlow",
      "year": "1988"
    },
    {
      "key": "2023072900595578400_Hilleretal1996",
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      "volume": "273",
      "author": "Hiller",
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      "first-page": "1896",
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      "article-title": "Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome",
      "volume": "94",
      "author": "Hughes",
      "year": "1997",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
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      "key": "2023072900595578400_HuppaandPloegh1997",
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      "first-page": "113",
      "DOI": "10.1016/S1074-7613(00)80514-2",
      "article-title": "The alpha chain of the T cell antigen receptor is degraded in the cytosol",
      "volume": "7",
      "author": "Huppa",
      "year": "1997",
      "journal-title": "Immunity"
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      "key": "2023072900595578400_Johnstonetal1998",
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      "first-page": "1883",
      "DOI": "10.1083/jcb.143.7.1883",
      "article-title": "Aggresomesa cellular response to misfolded proteins",
      "volume": "143",
      "author": "Johnston",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072900595578400_Jonesetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "4830",
      "DOI": "10.1128/jvi.69.8.4830-4841.1995",
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      "volume": "69",
      "author": "Jones",
      "year": "1995",
      "journal-title": "J. Virol."
    },
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      "key": "2023072900595578400_Kopito1997",
      "doi-asserted-by": "crossref",
      "first-page": "427",
      "DOI": "10.1016/S0092-8674(00)81881-4",
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      "volume": "88",
      "author": "Kopito",
      "year": "1997",
      "journal-title": "Cell"
    },
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      "first-page": "3251",
      "DOI": "10.1093/emboj/17.12.3251",
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      "volume": "17",
      "author": "Mayer",
      "year": "1998",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900595578400_McCrackenandBrodsky1996",
      "doi-asserted-by": "crossref",
      "first-page": "291",
      "DOI": "10.1083/jcb.132.3.291",
      "article-title": "Assembly of ER-associated protein degradation in vitrodependence on cytosol, calnexin, and ATP",
      "volume": "132",
      "author": "McCracken",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072900595578400_Neefjesetal1986",
      "doi-asserted-by": "crossref",
      "first-page": "164",
      "DOI": "10.1007/BF00373817",
      "article-title": "An analysis of class I antigens of man and other species by one-dimensional IEF and immunoblotting",
      "volume": "23",
      "author": "Neefjes",
      "year": "1986",
      "journal-title": "Immunogenetics"
    },
    {
      "key": "2023072900595578400_Pilonetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "4540",
      "DOI": "10.1093/emboj/16.15.4540",
      "article-title": "Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation",
      "volume": "16",
      "author": "Pilon",
      "year": "1997",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072900595578400_Plemperetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "891",
      "DOI": "10.1038/42276",
      "article-title": "Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation",
      "volume": "388",
      "author": "Plemper",
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      "volume": "271",
      "author": "Qu",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
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      "article-title": "Intracellular distribution of proteasomes",
      "volume": "10",
      "author": "Rivett",
      "year": "1998",
      "journal-title": "Curr. Opin. Immunol."
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      "author": "Sommer",
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      "first-page": "8516",
      "DOI": "10.1073/pnas.96.15.8516",
      "article-title": "The cytosolic tail of class I MHC heavy chain is required for its dislocation by the human cytomegalovirus US2 and US11 gene products",
      "volume": "96",
      "author": "Story",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072900595578400_SurdejandJacobs-Lorena1994",
      "first-page": "560",
      "article-title": "Strategy for epitope tagging the protein-coding region of any gene",
      "volume": "17",
      "author": "Surdej",
      "year": "1994",
      "journal-title": "Biotechniques."
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    {
      "key": "2023072900595578400_Suzukietal1994",
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      "first-page": "17611",
      "DOI": "10.1016/S0021-9258(17)32485-7",
      "article-title": "Purification and enzymatic properties of peptide:N-glycanase from C3H mouse-derived L-929 fibroblast cells. Possible widespread occurrence of post-translational remodification of proteins by N-deglycosylation",
      "volume": "269",
      "author": "Suzuki",
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      "journal-title": "J. Biol. Chem."
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      "first-page": "1357",
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      "article-title": "Retrograde transport from the Golgi region to the endoplasmic reticulum is sensitive to GTP gamma S",
      "volume": "116",
      "author": "Tan",
      "year": "1992",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072900595578400_Tortorellaetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "365",
      "DOI": "10.1083/jcb.142.2.365",
      "article-title": "Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential",
      "volume": "142",
      "author": "Tortorella",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072900595578400_vandeRijnetal1983",
      "doi-asserted-by": "crossref",
      "first-page": "525",
      "DOI": "10.1159/000131967",
      "article-title": "Localization of a gene controlling the expression of the human transferrin receptor to the region q12 leads to qter of chromosome 3",
      "volume": "36",
      "author": "van de Rijn",
      "year": "1983",
      "journal-title": "Cytogenet. Cell Genet."
    },
    {
      "key": "2023072900595578400_Wardetal1995",
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      "author": "Ward",
      "year": "1995",
      "journal-title": "Cell"
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      "first-page": "769",
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      "article-title": "The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol",
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      "author": "Wiertz",
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      "journal-title": "Cell"
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      "DOI": "10.1038/384432a0",
      "article-title": "Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction",
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      "article-title": "Cytosolic degradation of T-cell receptor alpha chains by the proteasome",
      "volume": "272",
      "author": "Yu",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
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      "volume": "123",
      "author": "Yuk",
      "year": "1993",
      "journal-title": "J. Cell Biol."
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