DOI: 10.1083/jcb.200312079. The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells

The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells

10.1083/jcb.200312079

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Protein translocons of the mammalian endoplasmic reticulum are composed of numerous functional components whose organization during different stages of the transport cycle in vivo remains poorly understood. We have developed generally applicable methods based on fluorescence resonance energy transfer (FRET) to probe the relative proximities of endogenously expressed translocon components in cells. Examination of substrate-engaged translocons revealed oligomeric assemblies of the Sec61 complex that were associated to varying degrees with other essential components including the signal recognition particle receptor TRAM and the TRAP complex. Remarkably, these components not only remained assembled but also had a similar, yet distinguishable, organization both during and after nascent chain translocation. The persistence of preassembled and complete translocons between successive rounds of transport may facilitate highly efficient translocation in vivo despite temporal constraints imposed by ongoing translation and a crowded cellular environment.

Bibliography

Snapp, E. L., Reinhart, G. A., Bogert, B. A., Lippincott-Schwartz, J., & Hegde, R. S. (2004). The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells. The Journal of Cell Biology, 164(7), 997â1007.

Authors 5

Erik L. Snapp (first)
Gretchen A. Reinhart (additional)
Brigitte A. Bogert (additional)
Jennifer Lippincott-Schwartz (additional)
Ramanujan S. Hegde (additional)

References 35 Referenced 76

10.1126/science.278.5346.2123 / Science. (1997)
10.1016/S0092-8674(01)00541-4 / Cell. (2001)
10.1016/0968-0004(94)90205-4 / Trends Biochem. Sci. (1994)
10.1016/0092-8674(94)90424-3 / Cell. (1994)
10.1083/jcb.200210095 / J. Cell Biol. (2003)
10.1016/0092-8674(93)90483-7 / Cell. (1993)
10.1016/0092-8674(92)90517-G / Cell. (1992)
10.1016/S0092-8674(00)80235-4 / Cell. (1997)
10.1016/S0092-8674(00)81403-8 / Cell. (1998)
10.1016/S0092-8674(00)81391-4 / Cell. (1996)
10.1006/meth.1998.0724 / Methods. (1999)
10.1146/annurev.cellbio.15.1.799 / Annu. Rev. Cell Dev. Biol. (1999)
10.1016/0092-8674(95)90313-5 / Cell. (1995)
10.1083/jcb.126.4.925 / J. Cell Biol. (1994)
10.1006/meth.2001.1189 / Methods. (2001)
10.1083/jcb.142.1.69 / J. Cell Biol. (1998)
10.1016/S0006-3495(93)81345-6 / Biophys. J. (1993)
10.1083/jcb.102.6.2015 / J. Cell Biol. (1986)
10.1083/jcb.200303143 / J. Cell Biol. (2003)
10.1074/jbc.270.11.6170 / J. Biol. Chem. (1995)
10.1016/S1097-2765(00)00118-0 / Mol. Cell. (2000)
10.1126/science.288.5464.331 / Science. (2000)
10.1016/S0022-2836(02)01111-7 / J. Mol. Biol. (2002)
10.1083/jcb.200201116 / J. Cell Biol. (2002)
10.1126/science.3961485 / Science. (1986)
10.1074/jbc.M202559200 / J. Biol. Chem. (2002)
10.1146/annurev.bi.65.070196.001415 / Annu. Rev. Biochem. (1996)
10.1091/mbc.01-10-0514 / Mol. Biol. Cell. (2002)
10.1074/jbc.M207295200 / J. Biol. Chem. (2003)
10.1016/0092-8674(91)90455-8 / Cell. (1991)
10.1038/nature02218 / Nature. (2004)
10.1083/jcb.134.1.25 / J. Cell Biol. (1996)
10.1146/annurev.cb.10.110194.000511 / Annu. Rev. Cell Biol. (1994)
10.1016/S0014-5793(99)01075-3 / FEBS Lett. (1999)
10.1091/mbc.01-10-0518 / Mol. Biol. Cell. (2002)

Dates

Type	When
Created	21 years, 4 months ago (March 29, 2004, 5:57 p.m.)
Deposited	2 years ago (July 22, 2023, 10:57 a.m.)
Indexed	2 days, 4 hours ago (Aug. 19, 2025, 6:21 a.m.)
Issued	21 years, 4 months ago (March 29, 2004)
Published	21 years, 4 months ago (March 29, 2004)
Published Online	21 years, 4 months ago (March 29, 2004)
Published Print	21 years, 4 months ago (March 29, 2004)

Funders 0

None

BibTeX

@article{Snapp_2004, title={The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells}, volume={164}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200312079}, DOI={10.1083/jcb.200312079}, number={7}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Snapp, Erik L. and Reinhart, Gretchen A. and Bogert, Brigitte A. and Lippincott-Schwartz, Jennifer and Hegde, Ramanujan S.}, year={2004}, month=mar, pages={997–1007} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        19
      ]
    ],
    "date-time": "2025-08-19T10:21:26Z",
    "timestamp": 1755598886844
  },
  "reference-count": 35,
  "publisher": "Rockefeller University Press",
  "issue": "7",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2004,
        3,
        29
      ]
    ]
  },
  "abstract": "<jats:p>Protein translocons of the mammalian endoplasmic reticulum are composed of numerous functional components whose organization during different stages of the transport cycle in vivo remains poorly understood. We have developed generally applicable methods based on fluorescence resonance energy transfer (FRET) to probe the relative proximities of endogenously expressed translocon components in cells. Examination of substrate-engaged translocons revealed oligomeric assemblies of the Sec61 complex that were associated to varying degrees with other essential components including the signal recognition particle receptor TRAM and the TRAP complex. Remarkably, these components not only remained assembled but also had a similar, yet distinguishable, organization both during and after nascent chain translocation. The persistence of preassembled and complete translocons between successive rounds of transport may facilitate highly efficient translocation in vivo despite temporal constraints imposed by ongoing translation and a crowded cellular environment.</jats:p>",
  "DOI": "10.1083/jcb.200312079",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2004,
        3,
        29
      ]
    ],
    "date-time": "2004-03-29T22:57:55Z",
    "timestamp": 1080601075000
  },
  "page": "997-1007",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 76,
  "title": "The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells",
  "prefix": "10.1083",
  "volume": "164",
  "author": [
    {
      "given": "Erik L.",
      "family": "Snapp",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892"
        }
      ]
    },
    {
      "given": "Gretchen A.",
      "family": "Reinhart",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892"
        }
      ]
    },
    {
      "given": "Brigitte A.",
      "family": "Bogert",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892"
        }
      ]
    },
    {
      "given": "Jennifer",
      "family": "Lippincott-Schwartz",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892"
        }
      ]
    },
    {
      "given": "Ramanujan S.",
      "family": "Hegde",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2004,
        3,
        29
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072214562666000_BIB1",
      "doi-asserted-by": "crossref",
      "first-page": "2123",
      "DOI": "10.1126/science.278.5346.2123",
      "volume": "278",
      "year": "1997",
      "journal-title": "Science."
    },
    {
      "key": "2023072214562666000_BIB2",
      "doi-asserted-by": "crossref",
      "first-page": "361",
      "DOI": "10.1016/S0092-8674(01)00541-4",
      "volume": "107",
      "year": "2001",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "124",
      "DOI": "10.1016/0968-0004(94)90205-4",
      "volume": "19",
      "year": "1994",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "2023072214562666000_BIB4",
      "doi-asserted-by": "crossref",
      "first-page": "461",
      "DOI": "10.1016/0092-8674(94)90424-3",
      "volume": "78",
      "year": "1994",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB5",
      "doi-asserted-by": "crossref",
      "first-page": "529",
      "DOI": "10.1083/jcb.200210095",
      "volume": "160",
      "year": "2003",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "615",
      "DOI": "10.1016/0092-8674(93)90483-7",
      "volume": "75",
      "year": "1993",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB7",
      "doi-asserted-by": "crossref",
      "first-page": "489",
      "DOI": "10.1016/0092-8674(92)90517-G",
      "volume": "71",
      "year": "1992",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "535",
      "DOI": "10.1016/S0092-8674(00)80235-4",
      "volume": "89",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB9",
      "doi-asserted-by": "crossref",
      "first-page": "747",
      "DOI": "10.1016/S0092-8674(00)81403-8",
      "volume": "92",
      "year": "1998",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "721",
      "DOI": "10.1016/S0092-8674(00)81391-4",
      "volume": "87",
      "year": "1996",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB11",
      "doi-asserted-by": "crossref",
      "first-page": "125",
      "DOI": "10.1006/meth.1998.0724",
      "volume": "17",
      "year": "1999",
      "journal-title": "Methods."
    },
    {
      "key": "2023072214562666000_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "799",
      "DOI": "10.1146/annurev.cellbio.15.1.799",
      "volume": "15",
      "year": "1999",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "2023072214562666000_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "261",
      "DOI": "10.1016/0092-8674(95)90313-5",
      "volume": "82",
      "year": "1995",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "925",
      "DOI": "10.1083/jcb.126.4.925",
      "volume": "126",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1006/meth.2001.1189",
      "volume": "24",
      "year": "2001",
      "journal-title": "Methods."
    },
    {
      "key": "2023072214562666000_BIB16",
      "doi-asserted-by": "crossref",
      "first-page": "69",
      "DOI": "10.1083/jcb.142.1.69",
      "volume": "142",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "110",
      "DOI": "10.1016/S0006-3495(93)81345-6",
      "volume": "64",
      "year": "1993",
      "journal-title": "Biophys. J."
    },
    {
      "key": "2023072214562666000_BIB18",
      "doi-asserted-by": "crossref",
      "first-page": "2015",
      "DOI": "10.1083/jcb.102.6.2015",
      "volume": "102",
      "year": "1986",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB19",
      "doi-asserted-by": "crossref",
      "first-page": "575",
      "DOI": "10.1083/jcb.200303143",
      "volume": "162",
      "year": "2003",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB20",
      "doi-asserted-by": "crossref",
      "first-page": "6170",
      "DOI": "10.1074/jbc.270.11.6170",
      "volume": "270",
      "year": "1995",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072214562666000_BIB21",
      "doi-asserted-by": "crossref",
      "first-page": "1219",
      "DOI": "10.1016/S1097-2765(00)00118-0",
      "volume": "6",
      "year": "2000",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072214562666000_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "331",
      "DOI": "10.1126/science.288.5464.331",
      "volume": "288",
      "year": "2000",
      "journal-title": "Science."
    },
    {
      "key": "2023072214562666000_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "871",
      "DOI": "10.1016/S0022-2836(02)01111-7",
      "volume": "324",
      "year": "2002",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072214562666000_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1083/jcb.200201116",
      "volume": "158",
      "year": "2002",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB25",
      "doi-asserted-by": "crossref",
      "first-page": "348",
      "DOI": "10.1126/science.3961485",
      "volume": "232",
      "year": "1986",
      "journal-title": "Science."
    },
    {
      "key": "2023072214562666000_BIB26",
      "doi-asserted-by": "crossref",
      "first-page": "23314",
      "DOI": "10.1074/jbc.M202559200",
      "volume": "277",
      "year": "2002",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072214562666000_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "271",
      "DOI": "10.1146/annurev.bi.65.070196.001415",
      "volume": "65",
      "year": "1996",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "2023072214562666000_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "1778",
      "DOI": "10.1091/mbc.01-10-0514",
      "volume": "13",
      "year": "2002",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072214562666000_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "4397",
      "DOI": "10.1074/jbc.M207295200",
      "volume": "278",
      "year": "2003",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072214562666000_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "371",
      "DOI": "10.1016/0092-8674(91)90455-8",
      "volume": "65",
      "year": "1991",
      "journal-title": "Cell."
    },
    {
      "key": "2023072214562666000_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "36",
      "DOI": "10.1038/nature02218",
      "volume": "427",
      "year": "2004",
      "journal-title": "Nature."
    },
    {
      "key": "2023072214562666000_BIB32",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1083/jcb.134.1.25",
      "volume": "134",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB33",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1146/annurev.cb.10.110194.000511",
      "volume": "10",
      "year": "1994",
      "journal-title": "Annu. Rev. Cell Biol."
    },
    {
      "key": "2023072214562666000_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "316",
      "DOI": "10.1016/S0014-5793(99)01075-3",
      "volume": "457",
      "year": "1999",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "2023072214562666000_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "2223",
      "DOI": "10.1091/mbc.01-10-0518",
      "volume": "13",
      "year": "2002",
      "journal-title": "Mol. Biol. Cell."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/164/7/997/1528765/jcb1647997.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/164/7/997/1528765/jcb1647997.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        22
      ]
    ],
    "date-time": "2023-07-22T14:57:12Z",
    "timestamp": 1690037832000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/164/7/997/33836/The-organization-of-engaged-and-quiescent"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2004,
        3,
        29
      ]
    ]
  },
  "references-count": 35,
  "journal-issue": {
    "issue": "7",
    "published-print": {
      "date-parts": [
        [
          2004,
          3,
          29
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.200312079",
  "relation": {
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.3410/f.1018444.208546",
        "asserted-by": "object"
      },
      {
        "id-type": "doi",
        "id": "10.3410/f.1018444.208464",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "1540-8140",
    "0021-9525"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2004,
        3,
        29
      ]
    ]
  }
}