DOI: 10.1126/science.273.5282.1725. ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway

ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway

10.1126/science.273.5282.1725

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Secretion of proteins is initiated by their uptake into the endoplasmic reticulum (ER), which possesses a proteolytic system able to degrade misfolded and nonassembled proteins. The ER degradation system was studied with yeast mutants defective in the breakdown of a mutated soluble vacuolar protein, carboxypeptidase yscY (CPY*). The ubiquitin-conjugating enzyme Ubc7p participated in the degradation process, which was mediated by the cytosolic 26 S proteasome. It is likely that CPY* entered the ER, was glycosylated, and was then transported back out of the ER lumen to the cytoplasmic side of the organelle, where it was conjugated with ubiquitin and degraded.

Bibliography

Hiller, M. M., Finger, A., Schweiger, M., & Wolf, D. H. (1996). ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway. Science, 273(5282), 1725â1728.

Authors 4

Mark M. Hiller (first)
Andreas Finger (additional)
Markus Schweiger (additional)
Dieter H. Wolf (additional)

References 40 Referenced 594

Pryer N. K., Wuestehube L. J., Schekman R., Annu. Rev. Biochem. 61, 471 (1992); (10.1146/annurev.bi.61.070192.002351) / Annu. Rev. Biochem. by Pryer N. K. (1992)
Gaut J. R., Hendershot L. M., Curr. Opin. Cell Biol. 5, 589 (1993). (10.1016/0955-0674(93)90127-C) / Curr. Opin. Cell Biol. by Gaut J. R. (1993)
Rothman J. E., Cell 59, 591 (1989); (10.1016/0092-8674(89)90005-6) / Cell by Rothman J. E. (1989)
10.1038/355033a0
Doms R. W., Lamb R. A., Rose J. K., Helenius A., Virology 193, 545 (1993); (10.1006/viro.1993.1164) / Virology by Doms R. W. (1993)
Hartl F. U., Hlodan R., Langer T., Trends Biochem. Sci. 19, 20 (1994). (10.1016/0968-0004(94)90169-4) / Trends Biochem. Sci. by Hartl F. U. (1994)
Bonifacino J. S., Klausner R. D., in Cellular Proteolytic Systems, , Ciechanover A., Schwartz A. L., Eds. (Wiley-Liss, New York, 1994), vol. 15, pp. 137-160. / Cellular Proteolytic Systems by Bonifacino J. S. (1994)
Lippincott S. J., Bonifacino J. S., Yuan L. C., Klausner R. D., Cell 54, 209 (1988); (10.1016/0092-8674(88)90553-3) / Cell by Lippincott S. J. (1988)
Klausner R. D., Sitia R., ibid. 62, 611 (1990); / ibid. by Klausner R. D. (1990)
Bonifacino J. S., Lippincott S. J., Curr. Opin. Cell Biol. 3, 592 (1991). (10.1016/0955-0674(91)90028-W) / Curr. Opin. Cell Biol. by Bonifacino J. S. (1991)
Ward C. L., Omura S., Kopito R. R., Cell 83, 121 (1995); (10.1016/0092-8674(95)90240-6) / Cell by Ward C. L. (1995)
Jensen T. J., et al., ibid., p. 129. / ibid. by Jensen T. J.
10.1111/j.1432-1033.1993.tb18410.x
Knop M., Finger A., Braun T., Hellmuth K., Wolf D. H., EMBO J. 15, 753 (1996). (10.1002/j.1460-2075.1996.tb00411.x) / EMBO J. by Knop M. (1996)
Hiller M. M. unpublished results.
Vassal A., Boulet A., Decoster E., Faye G., Biochim. Biophys. Acta 1132, 211 (1992). (10.1016/0167-4781(92)90015-R) / Biochim. Biophys. Acta by Vassal A. (1992)
Jungmann J., Reins H. A., Schobert C., Jentsch S., Nature 361, 369 (1993). (10.1038/361369a0) / Nature by Jungmann J. (1993)
Chen P., Johnson P., Sommer T., Jentsch S., Hochstrasser M., Cell 74, 357 (1993). (10.1016/0092-8674(93)90426-Q) / Cell by Chen P. (1993)
Sommer T., Jentsch S., Nature 365, 176 (1993). (10.1038/365176a0) / Nature by Sommer T. (1993)
Seufert W., Jentsch S., EMBO J. 9, 543 (1990). (10.1002/j.1460-2075.1990.tb08141.x) / EMBO J. by Seufert W. (1990)
Chau V., et al.., Science 243, 1576 (1989). (10.1126/science.2538923) / Science by Chau V. (1989)
Arnason T., Ellison M. J., Mol. Cell. Biol. 14, 7876 (1994). / Mol. Cell. Biol. by Arnason T. (1994)
Hochstrasser M., Ellison M. J., Chau V., Varshavsky A., Proc. Natl. Acad. Sci. U.S.A. 88, 4606 (1991). (10.1073/pnas.88.11.4606) / Proc. Natl. Acad. Sci. U.S.A. by Hochstrasser M. (1991)
Schork S. M., Thumm M., Wolf D. H., J. Biol. Chem. 270, 26446 (1995). (10.1074/jbc.270.44.26446) / J. Biol. Chem. by Schork S. M. (1995)
10.1016/0955-0674(95)80031-X
Hilt W., Wolf D. H., Trends Biochem. Sci. 21, 96 (1996). (10.1016/S0968-0004(96)10012-8) / Trends Biochem. Sci. by Hilt W. (1996)
Heinemeyer W., Kleinschmidt J. A., Saidowsky J., Escher C., Wolf D. H., EMBO J. 10, 555 (1991); (10.1002/j.1460-2075.1991.tb07982.x) / EMBO J. by Heinemeyer W. (1991)
Hilt W., Enenkel C., Gruhler A., Singer T., Wolf D. H., J. Biol. Chem. 268, 3479 (1993). (10.1016/S0021-9258(18)53719-4) / J. Biol. Chem. by Hilt W. (1993)
Heinemeyer W., Gruhler A., Möhrle V., Mahe Y., Wolf D. H., J. Biol. Chem. 268, 5115 (1993). (10.1016/S0021-9258(18)53509-2) / J. Biol. Chem. by Heinemeyer W. (1993)
Ghislain M., Udvardy A., Mann C., Nature 366, 358 (1993). (10.1038/366358a0) / Nature by Ghislain M. (1993)
Rubin D. M., et al.., ibid. 379, 655 (1996). / ibid. by Rubin D. M. (1996)
Rivett A. J., Knecht E., Curr. Biol. 3, 127 (1993); (10.1016/0960-9822(93)90173-L) / Curr. Biol. by Rivett A. J. (1993)
Palmer A., Mason G. G., Paramio J. M., Knecht E., Rivett A. J., Eur. J. Cell Biol. 64, 163 (1994); / Eur. J. Cell Biol. by Palmer A. (1994)
Vallon U., Kull U., Protoplasma 182, 15 (1994). (10.1007/BF01403684) / Protoplasma by Vallon U. (1994)
Schwartz A. L., Ciechanover A., Brandt R. A., Geuze H. J., EMBO J. 7, 2961 (1988). (10.1002/j.1460-2075.1988.tb03158.x) / EMBO J. by Schwartz A. L. (1988)
Römisch K., Schekman R., Proc. Natl. Acad. Sci. U.S.A. 89, 7227 (1992); (10.1073/pnas.89.15.7227) / Proc. Natl. Acad. Sci. U.S.A. by Römisch K. (1992)
Roelse J., Gromme M., Momburg F., Hammerling G., Neefjes J., J. Exp. Med. 180, 1591 (1994). (10.1084/jem.180.5.1591) / J. Exp. Med. by Roelse J. (1994)
Rose M. D., Misra L. M., Vogel J. P., Cell 57, 1211 (1989). (10.1016/0092-8674(89)90058-5) / Cell by Rose M. D. (1989)
McCracken A. A., Brodsky J. L., J. Cell Biol. 132, 291 (1996). (10.1083/jcb.132.3.291) / J. Cell Biol. by McCracken A. A. (1996)
10.1016/S0092-8674(00)81054-5

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 2:30 p.m.)
Deposited	1 year ago (Aug. 7, 2024, 7:40 a.m.)
Indexed	5 days, 17 hours ago (Aug. 24, 2025, 6:51 p.m.)
Issued	28 years, 11 months ago (Sept. 20, 1996)
Published	28 years, 11 months ago (Sept. 20, 1996)
Published Print	28 years, 11 months ago (Sept. 20, 1996)

Funders 0

None

BibTeX

@article{Hiller_1996, title={ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway}, volume={273}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.273.5282.1725}, DOI={10.1126/science.273.5282.1725}, number={5282}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Hiller, Mark M. and Finger, Andreas and Schweiger, Markus and Wolf, Dieter H.}, year={1996}, month=sep, pages={1725–1728} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        24
      ]
    ],
    "date-time": "2025-08-24T22:51:41Z",
    "timestamp": 1756075901068
  },
  "reference-count": 40,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5282",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1996,
        9,
        20
      ]
    ]
  },
  "abstract": "<jats:p>\n            Secretion of proteins is initiated by their uptake into the endoplasmic reticulum (ER), which possesses a proteolytic system able to degrade misfolded and nonassembled proteins. The ER degradation system was studied with yeast mutants defective in the breakdown of a mutated soluble vacuolar protein, carboxypeptidase yscY (CPY*). The ubiquitin-conjugating enzyme Ubc7p participated in the degradation process, which was mediated by the cytosolic 26\n            <jats:italic>S</jats:italic>\n            proteasome. It is likely that CPY* entered the ER, was glycosylated, and was then transported back out of the ER lumen to the cytoplasmic side of the organelle, where it was conjugated with ubiquitin and degraded.\n          </jats:p>",
  "DOI": "10.1126/science.273.5282.1725",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        27
      ]
    ],
    "date-time": "2006-10-27T18:30:41Z",
    "timestamp": 1161973841000
  },
  "page": "1725-1728",
  "source": "Crossref",
  "is-referenced-by-count": 594,
  "title": "ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway",
  "prefix": "10.1126",
  "volume": "273",
  "author": [
    {
      "given": "Mark M.",
      "family": "Hiller",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Institut f\u00fcr Biochemie der Universit\u00e4t Stuttgart, Pfaffenwaldring 55, D-70569 Stuttgart, Germany."
        }
      ]
    },
    {
      "given": "Andreas",
      "family": "Finger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Institut f\u00fcr Biochemie der Universit\u00e4t Stuttgart, Pfaffenwaldring 55, D-70569 Stuttgart, Germany."
        }
      ]
    },
    {
      "given": "Markus",
      "family": "Schweiger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Institut f\u00fcr Biochemie der Universit\u00e4t Stuttgart, Pfaffenwaldring 55, D-70569 Stuttgart, Germany."
        }
      ]
    },
    {
      "given": "Dieter H.",
      "family": "Wolf",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Institut f\u00fcr Biochemie der Universit\u00e4t Stuttgart, Pfaffenwaldring 55, D-70569 Stuttgart, Germany."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_3_1_2_2",
      "doi-asserted-by": "crossref",
      "first-page": "471",
      "DOI": "10.1146/annurev.bi.61.070192.002351",
      "volume": "61",
      "author": "Pryer N. K.",
      "year": "1992",
      "unstructured": "Pryer N. K., Wuestehube L. J., Schekman R., Annu. Rev. Biochem. 61, 471 (1992);",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "e_1_3_1_2_3",
      "doi-asserted-by": "crossref",
      "first-page": "589",
      "DOI": "10.1016/0955-0674(93)90127-C",
      "volume": "5",
      "author": "Gaut J. R.",
      "year": "1993",
      "unstructured": "Gaut J. R., Hendershot L. M., Curr. Opin. Cell Biol. 5, 589 (1993).",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "e_1_3_1_3_2",
      "doi-asserted-by": "crossref",
      "first-page": "591",
      "DOI": "10.1016/0092-8674(89)90005-6",
      "volume": "59",
      "author": "Rothman J. E.",
      "year": "1989",
      "unstructured": "Rothman J. E., Cell 59, 591 (1989);",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_1_3_3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/355033a0"
    },
    {
      "key": "e_1_3_1_3_4",
      "doi-asserted-by": "crossref",
      "first-page": "545",
      "DOI": "10.1006/viro.1993.1164",
      "volume": "193",
      "author": "Doms R. W.",
      "year": "1993",
      "unstructured": "Doms R. W., Lamb R. A., Rose J. K., Helenius A., Virology 193, 545 (1993);",
      "journal-title": "Virology"
    },
    {
      "key": "e_1_3_1_3_5",
      "doi-asserted-by": "crossref",
      "first-page": "20",
      "DOI": "10.1016/0968-0004(94)90169-4",
      "volume": "19",
      "author": "Hartl F. U.",
      "year": "1994",
      "unstructured": "Hartl F. U., Hlodan R., Langer T., Trends Biochem. Sci. 19, 20 (1994).",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "e_1_3_1_4_2",
      "first-page": "137",
      "volume-title": "Cellular Proteolytic Systems",
      "author": "Bonifacino J. S.",
      "year": "1994",
      "unstructured": "Bonifacino J. S., Klausner R. D., in Cellular Proteolytic Systems, , Ciechanover A., Schwartz A. L., Eds. (Wiley-Liss, New York, 1994), vol. 15, pp. 137-160."
    },
    {
      "key": "e_1_3_1_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "209",
      "DOI": "10.1016/0092-8674(88)90553-3",
      "volume": "54",
      "author": "Lippincott S. J.",
      "year": "1988",
      "unstructured": "Lippincott S. J., Bonifacino J. S., Yuan L. C., Klausner R. D., Cell 54, 209 (1988);",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_1_5_3",
      "first-page": "611",
      "volume": "62",
      "author": "Klausner R. D.",
      "year": "1990",
      "unstructured": "Klausner R. D., Sitia R., ibid. 62, 611 (1990);",
      "journal-title": "ibid."
    },
    {
      "key": "e_1_3_1_5_4",
      "doi-asserted-by": "crossref",
      "first-page": "592",
      "DOI": "10.1016/0955-0674(91)90028-W",
      "volume": "3",
      "author": "Bonifacino J. S.",
      "year": "1991",
      "unstructured": "Bonifacino J. S., Lippincott S. J., Curr. Opin. Cell Biol. 3, 592 (1991).",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "e_1_3_1_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.1016/0092-8674(95)90240-6",
      "volume": "83",
      "author": "Ward C. L.",
      "year": "1995",
      "unstructured": "Ward C. L., Omura S., Kopito R. R., Cell 83, 121 (1995);",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_1_6_3",
      "first-page": "129",
      "author": "Jensen T. J.",
      "unstructured": "Jensen T. J., et al., ibid., p. 129.",
      "journal-title": "ibid."
    },
    {
      "key": "e_1_3_1_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1993.tb18410.x"
    },
    {
      "key": "e_1_3_1_8_2",
      "doi-asserted-by": "crossref",
      "first-page": "753",
      "DOI": "10.1002/j.1460-2075.1996.tb00411.x",
      "volume": "15",
      "author": "Knop M.",
      "year": "1996",
      "unstructured": "Knop M., Finger A., Braun T., Hellmuth K., Wolf D. H., EMBO J. 15, 753 (1996).",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_1_9_2",
      "unstructured": "Hiller M. M. unpublished results."
    },
    {
      "key": "e_1_3_1_11_2",
      "doi-asserted-by": "crossref",
      "first-page": "211",
      "DOI": "10.1016/0167-4781(92)90015-R",
      "volume": "1132",
      "author": "Vassal A.",
      "year": "1992",
      "unstructured": "Vassal A., Boulet A., Decoster E., Faye G., Biochim. Biophys. Acta 1132, 211 (1992).",
      "journal-title": "Biochim. Biophys. Acta"
    },
    {
      "key": "e_1_3_1_12_2",
      "doi-asserted-by": "crossref",
      "first-page": "369",
      "DOI": "10.1038/361369a0",
      "volume": "361",
      "author": "Jungmann J.",
      "year": "1993",
      "unstructured": "Jungmann J., Reins H. A., Schobert C., Jentsch S., Nature 361, 369 (1993).",
      "journal-title": "Nature"
    },
    {
      "key": "e_1_3_1_13_2",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1016/0092-8674(93)90426-Q",
      "volume": "74",
      "author": "Chen P.",
      "year": "1993",
      "unstructured": "Chen P., Johnson P., Sommer T., Jentsch S., Hochstrasser M., Cell 74, 357 (1993).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_1_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "176",
      "DOI": "10.1038/365176a0",
      "volume": "365",
      "author": "Sommer T.",
      "year": "1993",
      "unstructured": "Sommer T., Jentsch S., Nature 365, 176 (1993).",
      "journal-title": "Nature"
    },
    {
      "key": "e_1_3_1_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "543",
      "DOI": "10.1002/j.1460-2075.1990.tb08141.x",
      "volume": "9",
      "author": "Seufert W.",
      "year": "1990",
      "unstructured": "Seufert W., Jentsch S., EMBO J. 9, 543 (1990).",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_1_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "1576",
      "DOI": "10.1126/science.2538923",
      "volume": "243",
      "author": "Chau V.",
      "year": "1989",
      "unstructured": "Chau V., et al.., Science 243, 1576 (1989).",
      "journal-title": "Science"
    },
    {
      "key": "e_1_3_1_17_2",
      "first-page": "7876",
      "volume": "14",
      "author": "Arnason T.",
      "year": "1994",
      "unstructured": "Arnason T., Ellison M. J., Mol. Cell. Biol. 14, 7876 (1994).",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "e_1_3_1_18_2",
      "doi-asserted-by": "crossref",
      "first-page": "4606",
      "DOI": "10.1073/pnas.88.11.4606",
      "volume": "88",
      "author": "Hochstrasser M.",
      "year": "1991",
      "unstructured": "Hochstrasser M., Ellison M. J., Chau V., Varshavsky A., Proc. Natl. Acad. Sci. U.S.A. 88, 4606 (1991).",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "e_1_3_1_19_2",
      "doi-asserted-by": "crossref",
      "first-page": "26446",
      "DOI": "10.1074/jbc.270.44.26446",
      "volume": "270",
      "author": "Schork S. M.",
      "year": "1995",
      "unstructured": "Schork S. M., Thumm M., Wolf D. H., J. Biol. Chem. 270, 26446 (1995).",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_1_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0955-0674(95)80031-X"
    },
    {
      "key": "e_1_3_1_20_3",
      "doi-asserted-by": "crossref",
      "first-page": "96",
      "DOI": "10.1016/S0968-0004(96)10012-8",
      "volume": "21",
      "author": "Hilt W.",
      "year": "1996",
      "unstructured": "Hilt W., Wolf D. H., Trends Biochem. Sci. 21, 96 (1996).",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "e_1_3_1_21_2",
      "doi-asserted-by": "crossref",
      "first-page": "555",
      "DOI": "10.1002/j.1460-2075.1991.tb07982.x",
      "volume": "10",
      "author": "Heinemeyer W.",
      "year": "1991",
      "unstructured": "Heinemeyer W., Kleinschmidt J. A., Saidowsky J., Escher C., Wolf D. H., EMBO J. 10, 555 (1991);",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_1_21_3",
      "doi-asserted-by": "crossref",
      "first-page": "3479",
      "DOI": "10.1016/S0021-9258(18)53719-4",
      "volume": "268",
      "author": "Hilt W.",
      "year": "1993",
      "unstructured": "Hilt W., Enenkel C., Gruhler A., Singer T., Wolf D. H., J. Biol. Chem. 268, 3479 (1993).",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_1_22_2",
      "doi-asserted-by": "crossref",
      "first-page": "5115",
      "DOI": "10.1016/S0021-9258(18)53509-2",
      "volume": "268",
      "author": "Heinemeyer W.",
      "year": "1993",
      "unstructured": "Heinemeyer W., Gruhler A., M\u00f6hrle V., Mahe Y., Wolf D. H., J. Biol. Chem. 268, 5115 (1993).",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_3_1_23_2",
      "doi-asserted-by": "crossref",
      "first-page": "358",
      "DOI": "10.1038/366358a0",
      "volume": "366",
      "author": "Ghislain M.",
      "year": "1993",
      "unstructured": "Ghislain M., Udvardy A., Mann C., Nature 366, 358 (1993).",
      "journal-title": "Nature"
    },
    {
      "key": "e_1_3_1_24_2",
      "first-page": "655",
      "volume": "379",
      "author": "Rubin D. M.",
      "year": "1996",
      "unstructured": "Rubin D. M., et al.., ibid. 379, 655 (1996).",
      "journal-title": "ibid."
    },
    {
      "key": "e_1_3_1_25_2",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1016/0960-9822(93)90173-L",
      "volume": "3",
      "author": "Rivett A. J.",
      "year": "1993",
      "unstructured": "Rivett A. J., Knecht E., Curr. Biol. 3, 127 (1993);",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "e_1_3_1_25_3",
      "first-page": "163",
      "volume": "64",
      "author": "Palmer A.",
      "year": "1994",
      "unstructured": "Palmer A., Mason G. G., Paramio J. M., Knecht E., Rivett A. J., Eur. J. Cell Biol. 64, 163 (1994);",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "e_1_3_1_25_4",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1007/BF01403684",
      "volume": "182",
      "author": "Vallon U.",
      "year": "1994",
      "unstructured": "Vallon U., Kull U., Protoplasma 182, 15 (1994).",
      "journal-title": "Protoplasma"
    },
    {
      "key": "e_1_3_1_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "2961",
      "DOI": "10.1002/j.1460-2075.1988.tb03158.x",
      "volume": "7",
      "author": "Schwartz A. L.",
      "year": "1988",
      "unstructured": "Schwartz A. L., Ciechanover A., Brandt R. A., Geuze H. J., EMBO J. 7, 2961 (1988).",
      "journal-title": "EMBO J."
    },
    {
      "key": "e_1_3_1_27_2",
      "doi-asserted-by": "crossref",
      "first-page": "7227",
      "DOI": "10.1073/pnas.89.15.7227",
      "volume": "89",
      "author": "R\u00f6misch K.",
      "year": "1992",
      "unstructured": "R\u00f6misch K., Schekman R., Proc. Natl. Acad. Sci. U.S.A. 89, 7227 (1992);",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "e_1_3_1_27_3",
      "doi-asserted-by": "crossref",
      "first-page": "1591",
      "DOI": "10.1084/jem.180.5.1591",
      "volume": "180",
      "author": "Roelse J.",
      "year": "1994",
      "unstructured": "Roelse J., Gromme M., Momburg F., Hammerling G., Neefjes J., J. Exp. Med. 180, 1591 (1994).",
      "journal-title": "J. Exp. Med."
    },
    {
      "key": "e_1_3_1_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "1211",
      "DOI": "10.1016/0092-8674(89)90058-5",
      "volume": "57",
      "author": "Rose M. D.",
      "year": "1989",
      "unstructured": "Rose M. D., Misra L. M., Vogel J. P., Cell 57, 1211 (1989).",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_1_29_2",
      "doi-asserted-by": "crossref",
      "first-page": "291",
      "DOI": "10.1083/jcb.132.3.291",
      "volume": "132",
      "author": "McCracken A. A.",
      "year": "1996",
      "unstructured": "McCracken A. A., Brodsky J. L., J. Cell Biol. 132, 291 (1996).",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "e_1_3_1_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81054-5"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.273.5282.1725",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        8,
        7
      ]
    ],
    "date-time": "2024-08-07T11:40:43Z",
    "timestamp": 1723030843000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.273.5282.1725"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1996,
        9,
        20
      ]
    ]
  },
  "references-count": 40,
  "journal-issue": {
    "issue": "5282",
    "published-print": {
      "date-parts": [
        [
          1996,
          9,
          20
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.273.5282.1725"
  ],
  "URL": "http://dx.doi.org/10.1126/science.273.5282.1725",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1996,
        9,
        20
      ]
    ]
  }
}