DOI: 10.1091/mbc.e06-06-0557. Hse1, a Component of the Yeast Hrs-STAM Ubiquitin-sorting Complex, Associates with Ubiquitin Peptidases and a Ligase to Control Sorting Efficiency into Multivesicular Bodies

Hse1, a Component of the Yeast Hrs-STAM Ubiquitin-sorting Complex, Associates with Ubiquitin Peptidases and a Ligase to Control Sorting Efficiency into Multivesicular Bodies

10.1091/mbc.e06-06-0557

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Ubiquitinated integral membrane proteins are delivered to the interior of the lysosome/vacuole for degradation. This process relies on specific ubiquitination of potential cargo and recognition of that Ub-cargo by sorting receptors at multiple compartments. We show that the endosomal Hse1-Vps27 sorting receptor binds to ubiquitin peptidases and the ubiquitin ligase Rsp5. Hse1 is linked to Rsp5 directly via a PY element within its C-terminus and through a novel protein Hua1, which recruits a complex of Rsp5, Rup1, and Ubp2. The SH3 domain of Hse1 also binds to the deubiquitinating protein Ubp7. Functional analysis shows that when both modes of Rsp5 association with Hse1 are altered, sorting of cargo that requires efficient ubiquitination for entry into the MVB is blocked, whereas sorting of cargo containing an in-frame addition of ubiquitin is normal. Further deletion of Ubp7 restores sorting of cargo when the Rsp5:Hse1 interaction is compromised suggesting that both ubiquitin ligases and peptidases associate with the Hse1-Vps27 sorting complex to control the ubiquitination status and sorting efficiency of cargo proteins. Additionally, we find that disruption of UBP2 and RUP1 inhibits MVB sorting of some cargos suggesting that Rsp5 requires association with Ubp2 to properly ubiquitinate cargo for efficient MVB sorting.

Bibliography

Ren, J., Kee, Y., Huibregtse, J. M., & Piper, R. C. (2007). Hse1, a Component of the Yeast Hrs-STAM Ubiquitin-sorting Complex, Associates with Ubiquitin Peptidases and a Ligase to Control Sorting Efficiency into Multivesicular Bodies. Molecular Biology of the Cell, 18(1), 324â335.

Authors 4

Jihui Ren (first)
Younghoon Kee (additional)
Jon M. Huibregtse (additional)
Robert C. Piper (additional)

References 79 Referenced 64

10.1074/jbc.M301326200 / J. Biol. Chem by Alwan H. A. (2003)
10.1002/yea.1052 / Yeast by Andreasson C. (2004)
10.1091/mbc.11.10.3365 / Mol. Biol. Cell by Amerik A. Y. (2000)
10.1074/jbc.M210843200 / J. Biol. Chem by Bache K. G. (2003)
10.1083/jcb.146.6.1227 / J. Cell Biol by Beck T. (1999)
10.1038/ncb815 / Nat. Cell Biol by Bilodeau P. S. (2002)
10.1074/jbc.M406654200 / J. Biol. Chem by Bilodeau P. S. (2004)
10.1083/jcb.200305007 / J. Cell Biol by Bilodeau P. S. (2003)
10.1091/mbc.e03-04-0202
10.1093/emboj/20.18.5187 / EMBO J by Borodovsky A. (2001)
10.1016/S1074-5521(02)00248-X / Chem. Biol by Borodovsky A. (2002)
10.1111/j.1600-0854.2004.00169.x / Traffic by Bowers K. (2004)
10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2 / Yeast by Brachmann C. B. (1998)
10.1091/mbc.e04-05-0420
10.1074/jbc.M409194200 / J. Biol. Chem by Burri L. (2004)
10.1083/jcb.133.3.529 / J. Cell Biol by Cooper A. A. (1996)
10.1083/jcb.122.1.53 / J. Cell Biol by Davis N. G. (1993)
10.1242/jcs.114.11.2167 / J. Cell Sci by de Melker A. A. (2001)
10.1091/mbc.12.2.421
10.1083/jcb.200309026 / J. Cell Biol by Dunn R. (2004)
10.1093/genetics/157.1.91 / Genetics by Gajewska B. (2001)
10.1038/nature02046 / Nature by Ghaemmaghami S. (2003)
10.1038/nature00935 / Nature by Giaever G. (2002)
10.1038/nrm1360 / Nat. Rev. Mol. Cell Biol by Gruenberg J. (2004)
10.1093/nar/30.6.e23 / Nucleic Acids Res by Gueldener U. (2002)
10.1083/jcb.153.4.649 / J. Cell Biol by Helliwell S. B. (2001)
10.1038/sj.emboj.7600137 / EMBO J by Hettema E. H. (2004)
10.1146/annurev.cellbio.19.110701.154617 / Annu. Rev. Cell Dev. Biol by Hicke L. (2003)
10.1038/ncb1354 / Nat. Cell Biol by Hoeller D. (2006)
10.1073/pnas.1933153100 / Proc. Natl. Acad. Sci. USA by Hoshikawa C. (2003)
10.1073/pnas.061034498 / Proc. Natl. Acad. Sci. USA by Ito T. (2001)
10.1016/0092-8674(92)90108-O / Cell by Kaelin W. G. (1992)
10.1074/jbc.M007251200 / J. Biol. Chem by Kato M. (2000)
10.1016/S0092-8674(01)00434-2 / Cell by Katzmann D. J. (2001)
10.1038/nrm973 / Nat. Rev. Mol. Cell Biol by Katzmann D. J. (2002)
10.1091/mbc.e03-07-0473
10.1038/sj.emboj.7600710 / EMBO J by Kee Y. (2005)
{'key': 'B38', 'author': 'Kee Y.', 'year': '2006', 'journal-title': 'J. Biol. Chem'} / J. Biol. Chem by Kee Y. (2006)
10.1093/jb/mvi001 / J. Biochem. (Tokyo) by Komada M. (2005)
10.1074/jbc.272.33.20538 / J. Biol. Chem by Komada M. (1997)
10.1101/gad.12.23.3663 / Genes Dev by Levkowitz G. (1998)
10.1074/jbc.275.1.367 / J. Biol. Chem by Lill N. L. (2000)
10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U / Yeast by Longtine M. S. (1998)
10.1083/jcb.200106056 / J. Cell Biol by Longva K. E. (2002)
10.1016/S1534-5807(03)00321-6 / Dev. Cell by Marchese A. (2003)
10.1083/jcb.200401141 / J. Cell Biol by McCullough J. (2004)
10.1016/j.cub.2005.11.073 / Curr. Biol by McCullough J. (2006)
10.1083/jcb.200602082 / J. Cell Biol by Millard S. M. (2006)
10.1091/mbc.e05-06-0560
10.1111/j.1600-0854.2006.00452.x / Traffic by Mizuno E. (2006)
10.1074/jbc.M306953200 / J. Biol. Chem by Nikko E. (2003)
10.1016/S0092-8674(00)81707-9 / Cell by Odorizzi G. (1998)
10.1091/mbc.e03-10-0727
10.1038/416451a / Nature by Polo S. (2002)
10.1016/S0955-0674(03)00080-2 / Curr. Opin. Cell Biol by Raiborg C. (2003)
10.1083/jcb.120.1.55 / J. Cell Biol by Raths S. (1993)
10.1091/mbc.3.12.1389
10.1038/ncb743 / Nat. Cell Biol by Reggiori F. (2002)
10.1038/13732 / Nat. Biotechnol by Rigaut G. (1999)
10.1083/jcb.137.7.1469 / J. Cell Biol by Roberg K. J. (1997)
10.1074/jbc.275.11.8143 / J. Biol. Chem by Roth A. F. (2000)
10.1042/BJ20050067 / Biochem. J by Row P. E. (2005)
10.1074/jbc.M512615200 / J. Biol. Chem by Row P. E. (2006)
10.1038/ncb1107 / Nat. Cell Biol by Scott P. M. (2004)
10.1074/jbc.M410325200 / J. Biol. Chem by Shcherbik N. (2004)
10.1016/0166-6851(88)90044-8 / Mol. Biochem. Parasitol by Smith D. B. (1988)
10.1074/jbc.M102945200 / J. Biol. Chem by Soetens O. (2001)
10.1152/physrev.00020.2005 / Physiol. Rev by Staub O. (2006)
10.1038/sj.emboj.7600984 / EMBO J by Stimpson H. E. (2006)
10.1074/jbc.274.27.19129 / J. Biol. Chem by Tanaka N. (1999)
10.1126/science.1064987 / Science by Tong A. H. (2002)
10.1074/jbc.274.53.38061 / J. Biol. Chem by Urbanowski J. L. (1999)
10.1034/j.1600-0854.2001.20905.x / Traffic by Urbanowski J. L. (2001)
10.1042/bse0410081 / Essays Biochem by Urbe S. (2005)
10.1128/MCB.21.10.3564-3575.2001 / Mol. Cell. Biol by Wang G. (2001)
10.1128/MCB.19.1.342 / Mol. Cell. Biol by Wang G. (1999)
10.1016/S0378-1119(98)00535-6 / Gene by Yashiroda H. (1998)
10.1016/0092-8674(94)90367-0 / Cell by Yu H. (1994)
10.1091/mbc.e04-06-0446

Dates

Type	When
Created	18 years, 9 months ago (Nov. 1, 2006, 8:44 p.m.)
Deposited	4 years ago (Aug. 4, 2021, 1:39 a.m.)
Indexed	1 month ago (July 28, 2025, 5:27 p.m.)
Issued	18 years, 7 months ago (Jan. 1, 2007)
Published	18 years, 7 months ago (Jan. 1, 2007)
Published Print	18 years, 7 months ago (Jan. 1, 2007)

Funders 0

None

BibTeX

@article{Ren_2007, title={Hse1, a Component of the Yeast Hrs-STAM Ubiquitin-sorting Complex, Associates with Ubiquitin Peptidases and a Ligase to Control Sorting Efficiency into Multivesicular Bodies}, volume={18}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e06-06-0557}, DOI={10.1091/mbc.e06-06-0557}, number={1}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Ren, Jihui and Kee, Younghoon and Huibregtse, Jon M. and Piper, Robert C.}, editor={Brodsky, Jeffrey}, year={2007}, month=jan, pages={324–335} }

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      "DOI": "10.1083/jcb.146.6.1227",
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      "year": "1999",
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      "doi-asserted-by": "crossref",
      "first-page": "534",
      "DOI": "10.1038/ncb815",
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      "year": "2002",
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      "doi-asserted-by": "crossref",
      "first-page": "54808",
      "DOI": "10.1074/jbc.M406654200",
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    {
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    {
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    {
      "key": "B10",
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      "first-page": "5187",
      "DOI": "10.1093/emboj/20.18.5187",
      "volume": "20",
      "author": "Borodovsky A.",
      "year": "2001",
      "journal-title": "EMBO J"
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "1149",
      "DOI": "10.1016/S1074-5521(02)00248-X",
      "volume": "9",
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      "year": "2002",
      "journal-title": "Chem. Biol"
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "194",
      "DOI": "10.1111/j.1600-0854.2004.00169.x",
      "volume": "5",
      "author": "Bowers K.",
      "year": "2004",
      "journal-title": "Traffic"
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    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "115",
      "DOI": "10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2",
      "volume": "14",
      "author": "Brachmann C. B.",
      "year": "1998",
      "journal-title": "Yeast"
    },
    {
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      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.e04-05-0420"
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      "volume": "279",
      "author": "Burri L.",
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    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "529",
      "DOI": "10.1083/jcb.133.3.529",
      "volume": "133",
      "author": "Cooper A. A.",
      "year": "1996",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "53",
      "DOI": "10.1083/jcb.122.1.53",
      "volume": "122",
      "author": "Davis N. G.",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "2167",
      "DOI": "10.1242/jcs.114.11.2167",
      "volume": "114",
      "author": "de Melker A. A.",
      "year": "2001",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "B19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.12.2.421"
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    {
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      "DOI": "10.1083/jcb.200309026",
      "volume": "165",
      "author": "Dunn R.",
      "year": "2004",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "91",
      "DOI": "10.1093/genetics/157.1.91",
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      "author": "Gajewska B.",
      "year": "2001",
      "journal-title": "Genetics"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "737",
      "DOI": "10.1038/nature02046",
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      "author": "Ghaemmaghami S.",
      "year": "2003",
      "journal-title": "Nature"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1038/nature00935",
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      "year": "2002",
      "journal-title": "Nature"
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      "doi-asserted-by": "crossref",
      "first-page": "317",
      "DOI": "10.1038/nrm1360",
      "volume": "5",
      "author": "Gruenberg J.",
      "year": "2004",
      "journal-title": "Nat. Rev. Mol. Cell Biol"
    },
    {
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1093/nar/30.6.e23",
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      "year": "2002",
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      "year": "2001",
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      "volume": "19",
      "author": "Hicke L.",
      "year": "2003",
      "journal-title": "Annu. Rev. Cell Dev. Biol"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "163",
      "DOI": "10.1038/ncb1354",
      "volume": "8",
      "author": "Hoeller D.",
      "year": "2006",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "11505",
      "DOI": "10.1073/pnas.1933153100",
      "volume": "100",
      "author": "Hoshikawa C.",
      "year": "2003",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "4569",
      "DOI": "10.1073/pnas.061034498",
      "volume": "98",
      "author": "Ito T.",
      "year": "2001",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "351",
      "DOI": "10.1016/0092-8674(92)90108-O",
      "volume": "70",
      "author": "Kaelin W. G.",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "37481",
      "DOI": "10.1074/jbc.M007251200",
      "volume": "275",
      "author": "Kato M.",
      "year": "2000",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "145",
      "DOI": "10.1016/S0092-8674(01)00434-2",
      "volume": "106",
      "author": "Katzmann D. J.",
      "year": "2001",
      "journal-title": "Cell"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "893",
      "DOI": "10.1038/nrm973",
      "volume": "3",
      "author": "Katzmann D. J.",
      "year": "2002",
      "journal-title": "Nat. Rev. Mol. Cell Biol"
    },
    {
      "key": "B36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.e03-07-0473"
    },
    {
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