DOI: 10.1091/mbc.e08-01-0080. Beclin 1 Forms Two Distinct Phosphatidylinositol 3-Kinase Complexes with Mammalian Atg14 and UVRAG

Beclin 1 Forms Two Distinct Phosphatidylinositol 3-Kinase Complexes with Mammalian Atg14 and UVRAG

10.1091/mbc.e08-01-0080

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Class III phosphatidylinositol 3-kinase (PI3-kinase) regulates multiple membrane trafficking. In yeast, two distinct PI3-kinase complexes are known: complex I (Vps34, Vps15, Vps30/Atg6, and Atg14) is involved in autophagy, and complex II (Vps34, Vps15, Vps30/Atg6, and Vps38) functions in the vacuolar protein sorting pathway. Atg14 and Vps38 are important in inducing both complexes to exert distinct functions. In mammals, the counterparts of Vps34, Vps15, and Vps30/Atg6 have been identified as Vps34, p150, and Beclin 1, respectively. However, orthologues of Atg14 and Vps38 remain unknown. We identified putative mammalian homologues of Atg14 and Vps38. The Vps38 candidate is identical to UV irradiation resistance-associated gene (UVRAG), which has been reported as a Beclin 1-interacting protein. Although both human Atg14 and UVRAG interact with Beclin 1 and Vps34, Atg14, and UVRAG are not present in the same complex. Although Atg14 is present on autophagic isolation membranes, UVRAG primarily associates with Rab9-positive endosomes. Silencing of human Atg14 in HeLa cells suppresses autophagosome formation. The coiled-coil region of Atg14 required for binding with Vps34 and Beclin 1 is essential for autophagy. These results suggest that mammalian cells have at least two distinct class III PI3-kinase complexes, which may function in different membrane trafficking pathways.

Bibliography

Itakura, E., Kishi, C., Inoue, K., & Mizushima, N. (2008). Beclin 1 Forms Two Distinct Phosphatidylinositol 3-Kinase Complexes with Mammalian Atg14 and UVRAG. Molecular Biology of the Cell, 19(12), 5360â5372.

Authors 4

Eisuke Itakura (first)
Chieko Kishi (additional)
Kinji Inoue (additional)
Noboru Mizushima (additional)

References 71 Referenced 975

10.1093/nar/25.17.3389 / Nucleic Acids Res by Altschul S. F. (1997)
10.1083/jcb.200109030 / J. Cell Biol by Barbero P. (2002)
10.1074/jbc.273.34.21883 / J. Biol. Chem by Berg T. O. (1998)
10.1083/jcb.200507002 / J. Cell Biol by Bjørkøy G. (2005)
10.1111/j.1432-1033.1997.0240a.x / Eur. J. Biochem by Blommaart E. F. (1997)
10.1083/jcb.130.4.781 / J. Cell Biol by Brown W. J. (1995)
10.1242/jcs.00090 / J. Cell Sci by Burda P. (2002)
10.1074/jbc.M507201200 / J. Biol. Chem by Byfield M. P. (2005)
10.1016/j.tcb.2003.12.002 / Trends Cell Biol by Cuervo A. M. (2004)
10.1083/jcb.130.4.797 / J. Cell Biol by Davidson H. W. (1995)
10.1038/sj.emboj.7600203 / EMBO J by Dove S. K. (2004)
10.1104/pp.106.093864 / Plant Physiol by Fujiki Y. (2007)
10.4161/auto.1.1.1542 / Autophagy by Furuya N. (2005)
10.1083/jcb.200108152 / J. Cell Biol by Futter C. E. (2001)
10.1128/MCB.00577-06 / Mol. Cell Biol by Gabriely G. (2007)
10.1083/jcb.200712064 / J. Cell Biol by Hara T. (2008)
10.1093/emboj/cdg062 / EMBO J by Hettema E. H. (2003)
10.1242/jcs.02833 / J. Cell Sci by Johnson E. E. (2006)
10.1016/S0968-0004(01)02039-4 / Trends Biochem. Sci by Jones D. T. (2002)
10.1016/j.bbrc.2007.02.150 / Biochem. Biophys. Res. Commun by Kabeya Y. (2007)
10.1093/emboj/19.21.5720 / EMBO J by Kabeya Y. (2000)
10.1074/jbc.273.35.22284 / J. Biol. Chem by Kametaka S. (1998)
10.1093/embo-reports/kve061 / EMBO Reports by Kihara A. (2001)
10.1083/jcb.152.3.519 / J. Cell Biol by Kihara A. (2001)
10.1083/jcb.152.1.51 / J. Cell Biol by Kim J. (2001)
10.1242/jcs.01620 / J. Cell Sci by Klionsky D. J. (2005)
10.1038/nrm2245 / Nat. Rev. Mol. Cell Biol by Klionsky D. J. (2007)
10.1083/jcb.200412022 / J. Cell Biol by Komatsu M. (2005)
10.1038/nature03029 / Nature by Kuma A. (2004)
10.4161/auto.4012 / Autophagy by Kuma A. (2007)
10.1016/S1534-5807(04)00099-1 / Dev. Cell by Levine B. (2004)
10.1038/ncb1426 / Nat. Cell Biol by Liang C. (2006)
10.4161/auto.3437 / Autophagy by Liang C. (2007)
10.1038/ncb1740 / Nat. Cell Biol by Liang C. (2008)
10.1038/45257 / Nature by Liang X. H. (1999)
10.1128/JVI.72.11.8586-8596.1998 / J. Virol by Liang X. H. (1998)
10.1242/jcs.02855 / J. Cell Sci by Lindmo K. (2006)
10.1002/j.1460-2075.1993.tb05701.x / EMBO J by Lombardi D. (1993)
10.1126/science.252.5009.1162 / Science by Lupas A. (1991)
10.1038/sj.emboj.7601689 / EMBO J by Maiuri M. C. (2007)
10.1038/nature05925 / Nature by Maria Fimia G. (2007)
10.1161/01.RES.0000261924.76669.36 / Circ. Res by Matsui Y. (2007)
10.1101/gad.1599207 / Genes Dev by Mizushima N. (2007)
10.1242/jcs.00381 / J. Cell Sci by Mizushima N. (2003)
10.1038/nature06639 / Nature by Mizushima N. (2008)
10.1093/emboj/18.14.3888 / EMBO J by Mizushima N. (1999)
10.1083/jcb.152.4.657 / J. Cell Biol by Mizushima N. (2001)
10.4161/auto.4600 / Autophagy by Mizushima N. (2007)
10.1074/jbc.M204736200 / J. Biol. Chem by Nice D. C. (2002)
10.1073/pnas.0506925102 / Proc. Natl. Acad. Sci. USA by Nobukuni T. (2005)
10.1111/j.1365-2443.2008.01188.x / Genes Cells by Obara K. (2008)
{'key': 'B52', 'author': 'Obara K.', 'year': '2008', 'journal-title': 'J. Biol. Chem'} / J. Biol. Chem by Obara K. (2008)
10.1091/mbc.e05-09-0841
10.1016/j.cell.2005.07.002 / Cell by Pattingre S. (2005)
10.1074/jbc.275.2.992 / J. Biol. Chem by Petiot A. (2000)
10.1172/JCI20039 / J. Clin. Invest by Qu X. (2003)
{'key': 'B57', 'first-page': '406', 'volume': '4', 'author': 'Saitou N.', 'year': '1987', 'journal-title': 'Mol. Biol. Evol'} / Mol. Biol. Evol by Saitou N. (1987)
10.1126/science.8385367 / Science by Schu P. V. (1993)
10.1002/j.1460-2075.1993.tb05867.x / EMBO J by Stack J. H. (1993)
10.1091/mbc.e04-02-0147
10.1093/emboj/20.21.5971 / EMBO J by Suzuki K. (2001)
10.1111/j.1365-2443.2007.01050.x / Genes Cells by Suzuki K. (2007)
10.1016/j.febslet.2007.01.096 / FEBS Lett by Suzuki K. (2007)
10.1016/j.cub.2005.07.035 / Curr. Biol by Takacs-Vellai K. (2005)
10.4161/auto.1.2.1697 / Autophagy by Tanida I. (2005)
10.1146/annurev.biochem.70.1.535 / Annu. Rev. Biochem by Vanhaesebroeck B. (2001)
10.1016/j.molcel.2008.06.001 / Mol. Cell by Wei Y. (2008)
10.1083/jcb.200112050 / J. Cell Biol by Wurmser A. E. (2002)
10.1242/jcs.03172 / J. Cell Sci by Young A. R. (2006)
10.1073/pnas.2436255100 / Proc. Natl. Acad. Sci. USA by Yue Z. (2003)
10.1242/jcs.02735 / J. Cell Sci by Zeng X. (2006)

Dates

Type	When
Created	16 years, 10 months ago (Oct. 8, 2008, 9:09 p.m.)
Deposited	5 years, 3 months ago (May 8, 2020, 9:20 p.m.)
Indexed	4 days, 6 hours ago (Aug. 31, 2025, 7:32 p.m.)
Issued	16 years, 9 months ago (Dec. 1, 2008)
Published	16 years, 9 months ago (Dec. 1, 2008)
Published Print	16 years, 9 months ago (Dec. 1, 2008)

Funders 0

None

BibTeX

@article{Itakura_2008, title={Beclin 1 Forms Two Distinct Phosphatidylinositol 3-Kinase Complexes with Mammalian Atg14 and UVRAG}, volume={19}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e08-01-0080}, DOI={10.1091/mbc.e08-01-0080}, number={12}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Itakura, Eisuke and Kishi, Chieko and Inoue, Kinji and Mizushima, Noboru}, editor={Subramani, Suresh}, year={2008}, month=dec, pages={5360–5372} }

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    {
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      "first-page": "511",
      "DOI": "10.1083/jcb.200109030",
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      "author": "Barbero P.",
      "year": "2002",
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    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "21883",
      "DOI": "10.1074/jbc.273.34.21883",
      "volume": "273",
      "author": "Berg T. O.",
      "year": "1998",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "603",
      "DOI": "10.1083/jcb.200507002",
      "volume": "171",
      "author": "Bj\u00f8rk\u00f8y G.",
      "year": "2005",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "240",
      "DOI": "10.1111/j.1432-1033.1997.0240a.x",
      "volume": "243",
      "author": "Blommaart E. F.",
      "year": "1997",
      "journal-title": "Eur. J. Biochem"
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "781",
      "DOI": "10.1083/jcb.130.4.781",
      "volume": "130",
      "author": "Brown W. J.",
      "year": "1995",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "3889",
      "DOI": "10.1242/jcs.00090",
      "volume": "115",
      "author": "Burda P.",
      "year": "2002",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "33076",
      "DOI": "10.1074/jbc.M507201200",
      "volume": "280",
      "author": "Byfield M. P.",
      "year": "2005",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "70",
      "DOI": "10.1016/j.tcb.2003.12.002",
      "volume": "14",
      "author": "Cuervo A. M.",
      "year": "2004",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "797",
      "DOI": "10.1083/jcb.130.4.797",
      "volume": "130",
      "author": "Davidson H. W.",
      "year": "1995",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "1922",
      "DOI": "10.1038/sj.emboj.7600203",
      "volume": "23",
      "author": "Dove S. K.",
      "year": "2004",
      "journal-title": "EMBO J"
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "1132",
      "DOI": "10.1104/pp.106.093864",
      "volume": "143",
      "author": "Fujiki Y.",
      "year": "2007",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "46",
      "DOI": "10.4161/auto.1.1.1542",
      "volume": "1",
      "author": "Furuya N.",
      "year": "2005",
      "journal-title": "Autophagy"
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "1251",
      "DOI": "10.1083/jcb.200108152",
      "volume": "155",
      "author": "Futter C. E.",
      "year": "2001",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "526",
      "DOI": "10.1128/MCB.00577-06",
      "volume": "27",
      "author": "Gabriely G.",
      "year": "2007",
      "journal-title": "Mol. Cell Biol"
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1083/jcb.200712064",
      "volume": "181",
      "author": "Hara T.",
      "year": "2008",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "548",
      "DOI": "10.1093/emboj/cdg062",
      "volume": "22",
      "author": "Hettema E. H.",
      "year": "2003",
      "journal-title": "EMBO J"
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "1219",
      "DOI": "10.1242/jcs.02833",
      "volume": "119",
      "author": "Johnson E. E.",
      "year": "2006",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "161",
      "DOI": "10.1016/S0968-0004(01)02039-4",
      "volume": "27",
      "author": "Jones D. T.",
      "year": "2002",
      "journal-title": "Trends Biochem. Sci"
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "405",
      "DOI": "10.1016/j.bbrc.2007.02.150",
      "volume": "356",
      "author": "Kabeya Y.",
      "year": "2007",
      "journal-title": "Biochem. Biophys. Res. Commun"
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "5720",
      "DOI": "10.1093/emboj/19.21.5720",
      "volume": "19",
      "author": "Kabeya Y.",
      "year": "2000",
      "journal-title": "EMBO J"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "22284",
      "DOI": "10.1074/jbc.273.35.22284",
      "volume": "273",
      "author": "Kametaka S.",
      "year": "1998",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "330",
      "DOI": "10.1093/embo-reports/kve061",
      "volume": "2",
      "author": "Kihara A.",
      "year": "2001",
      "journal-title": "EMBO Reports"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "519",
      "DOI": "10.1083/jcb.152.3.519",
      "volume": "152",
      "author": "Kihara A.",
      "year": "2001",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "51",
      "DOI": "10.1083/jcb.152.1.51",
      "volume": "152",
      "author": "Kim J.",
      "year": "2001",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "7",
      "DOI": "10.1242/jcs.01620",
      "volume": "118",
      "author": "Klionsky D. J.",
      "year": "2005",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "931",
      "DOI": "10.1038/nrm2245",
      "volume": "8",
      "author": "Klionsky D. J.",
      "year": "2007",
      "journal-title": "Nat. Rev. Mol. Cell Biol"
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "425",
      "DOI": "10.1083/jcb.200412022",
      "volume": "169",
      "author": "Komatsu M.",
      "year": "2005",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "1032",
      "DOI": "10.1038/nature03029",
      "volume": "432",
      "author": "Kuma A.",
      "year": "2004",
      "journal-title": "Nature"
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "323",
      "DOI": "10.4161/auto.4012",
      "volume": "3",
      "author": "Kuma A.",
      "year": "2007",
      "journal-title": "Autophagy"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "463",
      "DOI": "10.1016/S1534-5807(04)00099-1",
      "volume": "6",
      "author": "Levine B.",
      "year": "2004",
      "journal-title": "Dev. Cell"
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "688",
      "DOI": "10.1038/ncb1426",
      "volume": "8",
      "author": "Liang C.",
      "year": "2006",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "69",
      "DOI": "10.4161/auto.3437",
      "volume": "3",
      "author": "Liang C.",
      "year": "2007",
      "journal-title": "Autophagy"
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "776",
      "DOI": "10.1038/ncb1740",
      "volume": "10",
      "author": "Liang C.",
      "year": "2008",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "672",
      "DOI": "10.1038/45257",
      "volume": "402",
      "author": "Liang X. H.",
      "year": "1999",
      "journal-title": "Nature"
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "8586",
      "DOI": "10.1128/JVI.72.11.8586-8596.1998",
      "volume": "72",
      "author": "Liang X. H.",
      "year": "1998",
      "journal-title": "J. Virol"
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