DOI: 10.1091/mbc.12.6.1885. Yeast Gga Coat Proteins Function with Clathrin in Golgi to Endosome Transport

Yeast Gga Coat Proteins Function with Clathrin in Golgi to Endosome Transport

10.1091/mbc.12.6.1885

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Gga proteins represent a newly recognized, evolutionarily conserved protein family with homology to the “ear” domain of the clathrin adaptor AP-1 γ subunit. Yeast cells contain two Gga proteins, Gga1p and Gga2p, that have been proposed to act in transport between thetrans-Golgi network and endosomes. Here we provide genetic and physical evidence that yeast Gga proteins function in trans-Golgi network clathrin coats. Deletion of Gga2p (gga2Δ), the major Gga protein, accentuates growth and α-factor maturation defects in cells carrying a temperature-sensitive allele of the clathrin heavy chain gene. Cells carrying eithergga2Δ or a deletion of the AP-1 β subunit gene(apl2Δ) alone are phenotypically normal, but cells carrying both gga2Δ andapl2Δ are defective in growth, α-factor maturation, and transport of carboxypeptidase S to the vacuole. Disruption of bothGGA genes and APL2 results in cells so severely compromised in growth that they form only microcolonies. Gga proteins can bind clathrin in vitro and cofractionate with clathrin-coated vesicles. Our results indicate that yeast Gga proteins play an important role in cargo-selective clathrin-mediated protein traffic from the trans-Golgi network to endosomes.

Bibliography

Costaguta, G., Stefan, C. J., Bensen, E. S., Emr, S. D., & Payne, G. S. (2001). Yeast Gga Coat Proteins Function with Clathrin in Golgi to Endosome Transport. Molecular Biology of the Cell, 12(6), 1885â1896.

Authors 5

G. Costaguta (first)
C. J. Stefan (additional)
E. S. Bensen (additional)
S. D. Emr (additional)
G. S. Payne (additional)

References 70 Referenced 118

10.1002/j.1460-2075.1988.tb02897.x / EMBO J. by Ahle S. (1988)
10.1093/genetics/154.1.83 / Genetics by Bensen E.S. (2000)
10.1083/jcb.151.3.587 / J. Cell Biol. by Black M.W. (2000)
10.1091/mbc.11.4.1241
10.1083/jcb.136.2.287 / J. Cell Biol. by Bryant N.J. (1997)
10.1016/0003-2697(81)90281-5 / Anal. Biochem. by Burnette W.N. (1981)
10.1091/mbc.6.9.1089
10.1016/S0955-0674(99)80067-2 / Curr. Opin. Cell Biol. by Chavrier P. (1999)
10.1093/genetics/150.2.577 / Genetics by Chen C.Y. (1998)
10.1074/jbc.271.51.33123 / J. Biol. Chem. by Chu D.S. (1996)
10.1016/S0167-4889(98)00058-5 / Biochim. Biophys. Acta by Conibear E. (1998)
10.1016/S0092-8674(01)80013-1 / Cell. by Cowles C.R. (1997)
10.1093/emboj/16.10.2769 / EMBO J. by Cowles C.R. (1997)
10.1126/science.280.5362.431 / Science by Dell'Angelica E.C. (1998)
10.1074/jbc.274.11.7278 / J. Biol. Chem. by Dell'Angelica E.C. (1999)
10.1093/emboj/16.5.917 / EMBO J. by Dell'Angelica E.C. (1997)
10.1083/jcb.149.1.81 / J. Cell Biol. by Dell'Angelica E.C. (2000)
10.1016/S1097-2765(00)80170-7 / Mol. Cell. by Dell'Angelica E.C. (1999)
10.1016/S0955-0674(00)00119-8 / Curr. Opin. Cell Biol. by Donaldson J.G. (2000)
10.1146/annurev.ph.50.030188.002021 / Annu. Rev. Physiol. by Fuller R.S. (1988)
10.1002/j.1460-2075.1993.tb06219.x / EMBO J. by Gallusser A. (1993)
10.1016/0168-9525(93)90042-G / Trends Genet. by Guarente L. (1993)
10.1091/mbc.10.8.2787
10.1083/jcb.149.1.67 / J. Cell Biol. by Hirst J. (2000)
10.1016/S0167-4889(98)00056-1 / Biochim. Biophys. Acta by Hirst J. (1998)
10.1093/emboj/18.14.3897 / EMBO J. by Huang K.M. (1999)
10.1146/annurev.cellbio.15.1.705 / Annu. Rev. Cell Dev. Biol. by Kirchhausen T. (1999)
10.1038/227680a0 / Nature by Laemmli U.K. (1970)
10.1016/S0014-5793(98)01401-X / FEBS Lett. by Lohi O. (1998)
10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U / Yeast by Longtine M.S. (1998)
10.1016/0092-8674(94)90219-4 / Cell by Marcusson E.G. (1994)
10.1126/science.285.5425.215 / Science by Marsh M. (1999)
10.1523/JNEUROSCI.20-23-08667.2000 / J. Neurosci. by Morgan J.R. (2000)
10.1016/S0092-8674(00)81707-9 / Cell by Odorizzi G. (1998)
10.1126/science.7569928 / Science by Ohno H. (1995)
10.1126/science.282.5392.1327 / Science by Owen D.J. (1998)
10.1016/S0092-8674(00)80791-6 / Cell by Owen D.J. (1999)
10.1093/emboj/19.16.4216 / EMBO J. by Owen D.J. (2000)
10.1093/emboj/16.14.4194 / EMBO J. by Panek H.R. (1997)
10.1126/science.2675311 / Science by Payne G.S. (1989)
10.1002/j.1460-2075.1994.tb06435.x / EMBO J. by Phan H.L. (1994)
10.1083/jcb.131.3.603 / J. Cell Biol. by Piper R.C. (1995)
10.1038/35046619 / Nat. Cell. Biol. by Pishvaee B. (2000)
10.1016/S0092-8674(00)81611-6 / Cell by Pishvaee B. (1998)
10.1074/jbc.275.10.7176 / J. Biol. Chem. by Poussu A. (2000)
10.1242/jcs.108.4.1605 / J. Cell Sci. by Rad M.R. (1995)
10.1093/emboj/17.8.2148 / EMBO J. by Rapoport I. (1998)
10.1091/mbc.3.12.1389
10.1091/mbc.7.6.985
10.1128/MCB.8.11.4936 / Mol. Cell. Biol. by Robinson J.S. (1988)
10.1083/jcb.104.4.887 / J. Cell Biol. by Robinson M.S. (1987)
10.1083/jcb.102.1.48 / J. Cell Biol. by Robinson M.S. (1986)
10.1146/annurev.biochem.66.1.511 / Annu. Rev. Biochem. by Schmid S.L. (1997)
10.1083/jcb.137.1.79 / J. Cell Biol. by Seaman M.N. (1997)
10.1083/jcb.118.3.531 / J. Cell Biol. by Seeger M. (1992)
10.1093/genetics/122.1.19 / Genetics by Sikorski R.S. (1989)
10.1083/jcb.133.4.749 / J. Cell Biol. by Simpson F. (1996)
10.1083/jcb.137.4.835 / J. Cell Biol. by Simpson F. (1997)
10.1091/mbc.6.1.41
10.1006/bbrc.2000.2700 / Biochem. Biophys. Res. Commun. by Takatsu H. (2000)
10.1083/jcb.123.6.1707 / J. Cell Biol. by Tan P.K. (1993)
10.1073/pnas.97.3.1096 / Proc. Natl. Acad. Sci. USA by ter Haar E. (2000)
10.1073/pnas.96.16.8907 / Proc. Natl. Acad. Sci. USA by Traub L.M. (1999)
10.1083/jcb.128.5.779 / J. Cell Biol. by Vida T.A. (1995)
10.1093/emboj/17.9.2482 / EMBO J. by Vowels J.J. (1998)
10.1083/jcb.141.1.71 / J. Cell Biol. by Wendland B. (1998)
10.1093/emboj/18.16.4383 / EMBO J. by Wendland B. (1999)
10.1091/mbc.10.11.3643
10.1002/1097-0061(200101)18:1<1::AID-YEA644>3.0.CO;2-5 / Yeast by Zhdankina O. (2001)
10.1074/jbc.275.18.13465 / J. Biol. Chem. by Zhu X. (2000)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 8:15 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:45 p.m.)
Indexed	1 year, 3 months ago (May 22, 2024, 9:14 a.m.)
Issued	24 years, 2 months ago (June 1, 2001)
Published	24 years, 2 months ago (June 1, 2001)
Published Print	24 years, 2 months ago (June 1, 2001)

Funders 0

None

BibTeX

@article{Costaguta_2001, title={Yeast Gga Coat Proteins Function with Clathrin in Golgi to Endosome Transport}, volume={12}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.12.6.1885}, DOI={10.1091/mbc.12.6.1885}, number={6}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Costaguta, G. and Stefan, C. J. and Bensen, E. S. and Emr, S. D. and Payne, G. S.}, editor={Riezman, Howard}, year={2001}, month=jun, pages={1885–1896} }

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  "abstract": "<jats:p>Gga proteins represent a newly recognized, evolutionarily conserved protein family with homology to the \u201cear\u201d domain of the clathrin adaptor AP-1 \u03b3 subunit. Yeast cells contain two Gga proteins, Gga1p and Gga2p, that have been proposed to act in transport between thetrans-Golgi network and endosomes. Here we provide genetic and physical evidence that yeast Gga proteins function in trans-Golgi network clathrin coats. Deletion of Gga2p (gga2\u0394), the major Gga protein, accentuates growth and \u03b1-factor maturation defects in cells carrying a temperature-sensitive allele of the clathrin heavy chain gene. Cells carrying eithergga2\u0394 or a deletion of the AP-1 \u03b2 subunit gene(apl2\u0394) alone are phenotypically normal, but cells carrying both gga2\u0394 andapl2\u0394 are defective in growth, \u03b1-factor maturation, and transport of carboxypeptidase S to the vacuole. Disruption of bothGGA genes and APL2 results in cells so severely compromised in growth that they form only microcolonies. Gga proteins can bind clathrin in vitro and cofractionate with clathrin-coated vesicles. Our results indicate that yeast Gga proteins play an important role in cargo-selective clathrin-mediated protein traffic from the trans-Golgi network to endosomes.</jats:p>",
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      "volume": "151",
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      "journal-title": "J. Cell Biol."
    },
    {
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      "DOI": "10.1083/jcb.136.2.287",
      "volume": "136",
      "author": "Bryant N.J.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "195",
      "DOI": "10.1016/0003-2697(81)90281-5",
      "volume": "112",
      "author": "Burnette W.N.",
      "year": "1981",
      "journal-title": "Anal. Biochem."
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    {
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      "first-page": "466",
      "DOI": "10.1016/S0955-0674(99)80067-2",
      "volume": "11",
      "author": "Chavrier P.",
      "year": "1999",
      "journal-title": "Curr. Opin. Cell Biol."
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    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "577",
      "DOI": "10.1093/genetics/150.2.577",
      "volume": "150",
      "author": "Chen C.Y.",
      "year": "1998",
      "journal-title": "Genetics"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "33123",
      "DOI": "10.1074/jbc.271.51.33123",
      "volume": "271",
      "author": "Chu D.S.",
      "year": "1996",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "211",
      "DOI": "10.1016/S0167-4889(98)00058-5",
      "volume": "1404",
      "author": "Conibear E.",
      "year": "1998",
      "journal-title": "Biochim. Biophys. Acta"
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1016/S0092-8674(01)80013-1",
      "volume": "91",
      "author": "Cowles C.R.",
      "year": "1997",
      "journal-title": "Cell."
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    {
      "key": "B13",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1093/emboj/16.10.2769",
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      "first-page": "431",
      "DOI": "10.1126/science.280.5362.431",
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      "year": "1998",
      "journal-title": "Science"
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    {
      "key": "B15",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1074/jbc.274.11.7278",
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      "year": "1999",
      "journal-title": "J. Biol. Chem."
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    {
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      "journal-title": "EMBO J."
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      "first-page": "81",
      "DOI": "10.1083/jcb.149.1.81",
      "volume": "149",
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      "year": "2000",
      "journal-title": "J. Cell Biol."
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    {
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      "doi-asserted-by": "crossref",
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      "year": "1999",
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      "key": "B19",
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      "journal-title": "Curr. Opin. Cell Biol."
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      "key": "B20",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1146/annurev.ph.50.030188.002021",
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      "author": "Fuller R.S.",
      "year": "1988",
      "journal-title": "Annu. Rev. Physiol."
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1002/j.1460-2075.1993.tb06219.x",
      "volume": "12",
      "author": "Gallusser A.",
      "year": "1993",
      "journal-title": "EMBO J."
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "362",
      "DOI": "10.1016/0168-9525(93)90042-G",
      "volume": "9",
      "author": "Guarente L.",
      "year": "1993",
      "journal-title": "Trends Genet."
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    {
      "key": "B23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.10.8.2787"
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      "DOI": "10.1083/jcb.149.1.67",
      "volume": "149",
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      "year": "2000",
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    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "173",
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      "key": "B26",
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      "volume": "15",
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      "doi-asserted-by": "crossref",
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    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "255",
      "DOI": "10.1016/S0014-5793(98)01401-X",
      "volume": "440",
      "author": "Lohi O.",
      "year": "1998",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "953",
      "DOI": "10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U",
      "volume": "14",
      "author": "Longtine M.S.",
      "year": "1998",
      "journal-title": "Yeast"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1016/0092-8674(94)90219-4",
      "volume": "77",
      "author": "Marcusson E.G.",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "215",
      "DOI": "10.1126/science.285.5425.215",
      "volume": "285",
      "author": "Marsh M.",
      "year": "1999",
      "journal-title": "Science"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "8667",
      "DOI": "10.1523/JNEUROSCI.20-23-08667.2000",
      "volume": "20",
      "author": "Morgan J.R.",
      "year": "2000",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "847",
      "DOI": "10.1016/S0092-8674(00)81707-9",
      "volume": "95",
      "author": "Odorizzi G.",
      "year": "1998",
      "journal-title": "Cell"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "1872",
      "DOI": "10.1126/science.7569928",
      "volume": "269",
      "author": "Ohno H.",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "1327",
      "DOI": "10.1126/science.282.5392.1327",
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