DOI: 10.1083/jcb.200707010. Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies

Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies

10.1083/jcb.200707010

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Cytoplasmic RNA granules serve key functions in the control of messenger RNA (mRNA) fate in eukaryotic cells. For instance, in yeast, severe stress induces mRNA relocalization to sites of degradation or storage called processing bodies (P-bodies). In this study, we show that the translation repression associated with glucose starvation causes the key translational mediators of mRNA recognition, eIF4E, eIF4G, and Pab1p, to resediment away from ribosomal fractions. These mediators then accumulate in P-bodies and in previously unrecognized cytoplasmic bodies, which we define as EGP-bodies. Our kinetic studies highlight the fundamental difference between EGP- and P-bodies and reflect the complex dynamics surrounding reconfiguration of the mRNA pool under stress conditions. An absence of key mRNA decay factors from EGP-bodies points toward an mRNA storage function for these bodies. Overall, this study highlights new potential control points in both the regulation of mRNA fate and the global control of translation initiation.

Bibliography

Hoyle, N. P., Castelli, L. M., Campbell, S. G., Holmes, L. E. A., & Ashe, M. P. (2007). Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. The Journal of Cell Biology, 179(1), 65â74.

Authors 5

Nathaniel P. Hoyle (first)
Lydia M. Castelli (additional)
Susan G. Campbell (additional)
Leah E.A. Holmes (additional)
Mark P. Ashe (additional)

References 39 Referenced 211

10.1093/emboj/16.5.1114 / EMBO J. (1997)
10.1083/jcb.200512082 / J. Cell Biol. (2006)
10.1261/rna.2340405 / RNA. (2005)
10.1091/mbc.11.3.833 / Mol. Biol. Cell. (2000)
10.1093/emboj/20.22.6464 / EMBO J. (2001)
10.1091/mbc.e06-12-1149 / Mol. Biol. Cell. (2007)
10.1126/science.1115791 / Science. (2005)
10.1017/S1355838200001059 / RNA. (2000)
{'key': '2023072911400904900_BIB9', 'year': '2000'} (2000)
10.1083/jcb.200503162 / J. Cell Biol. (2005)
10.1016/j.cell.2005.02.024 / Cell. (2005)
10.1083/jcb.200309008 / J. Cell Biol. (2004)
10.1083/jcb.200504039 / J. Cell Biol. (2005)
10.1002/j.1460-2075.1994.tb06699.x / EMBO J. (1994)
10.1146/annurev.micro.59.031805.133833 / Annu. Rev. Microbiol. (2005)
10.1128/MCB.24.7.2998-3010.2004 / Mol. Cell. Biol. (2004)
10.1002/yea.1415 / Yeast. (2006)
10.1002/yea.1142 / Yeast. (2004)
10.1016/j.molcel.2006.11.028 / Mol. Cell. (2007)
10.1146/annurev.biochem.73.030403.080419 / Annu. Rev. Biochem. (2004)
10.1042/bst0300963 / Biochem. Soc. Trans. (2002)
10.1083/jcb.147.7.1431 / J. Cell Biol. (1999)
10.1083/jcb.200502088 / J. Cell Biol. (2005)
10.1016/j.cell.2007.05.016 / Cell. (2007)
10.1016/S0074-7696(01)03007-8 / Int. Rev. Cytol. (2001)
10.1016/S1097-2765(00)80282-8 / Mol. Cell. (1998)
10.1128/MCB.21.13.4347-4368.2001 / Mol. Cell. Biol. (2001)
10.1128/MCB.19.8.5557 / Mol. Cell. Biol. (1999)
10.1038/sj.emboj.7600116 / EMBO J. (2004)
10.1016/j.molcel.2007.02.011 / Mol. Cell. (2007)
10.1038/nature03205 / Nature. (2005)
{'key': '2023072911400904900_BIB32', 'year': '2000'} (2000)
{'key': '2023072911400904900_BIB33', 'year': '2000'} (2000)
10.1126/science.1082320 / Science. (2003)
10.1016/j.cell.2006.04.037 / Cell. (2006)
10.1128/MCB.25.21.9340-9349.2005 / Mol. Cell. Biol. (2005)
10.1073/pnas.79.5.1558 / Proc. Natl. Acad. Sci. USA. (1982)
10.1261/rna.7258505 / RNA. (2005)
10.1046/j.1365-2958.2002.03172.x / Mol. Microbiol. (2002)

Dates

Type	When
Created	17 years, 11 months ago (Oct. 1, 2007, 8:26 p.m.)
Deposited	2 years, 1 month ago (July 29, 2023, 7:41 a.m.)
Indexed	1 month, 1 week ago (July 22, 2025, 7:16 a.m.)
Issued	17 years, 11 months ago (Oct. 1, 2007)
Published	17 years, 11 months ago (Oct. 1, 2007)
Published Online	17 years, 11 months ago (Oct. 1, 2007)
Published Print	17 years, 10 months ago (Oct. 8, 2007)

Funders 0

None

BibTeX

@article{Hoyle_2007, title={Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies}, volume={179}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200707010}, DOI={10.1083/jcb.200707010}, number={1}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Hoyle, Nathaniel P. and Castelli, Lydia M. and Campbell, Susan G. and Holmes, Leah E.A. and Ashe, Mark P.}, year={2007}, month=oct, pages={65–74} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        22
      ]
    ],
    "date-time": "2025-07-22T11:16:02Z",
    "timestamp": 1753182962523
  },
  "reference-count": 39,
  "publisher": "Rockefeller University Press",
  "issue": "1",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        10,
        8
      ]
    ]
  },
  "abstract": "<jats:p>Cytoplasmic RNA granules serve key functions in the control of messenger RNA (mRNA) fate in eukaryotic cells. For instance, in yeast, severe stress induces mRNA relocalization to sites of degradation or storage called processing bodies (P-bodies). In this study, we show that the translation repression associated with glucose starvation causes the key translational mediators of mRNA recognition, eIF4E, eIF4G, and Pab1p, to resediment away from ribosomal fractions. These mediators then accumulate in P-bodies and in previously unrecognized cytoplasmic bodies, which we define as EGP-bodies. Our kinetic studies highlight the fundamental difference between EGP- and P-bodies and reflect the complex dynamics surrounding reconfiguration of the mRNA pool under stress conditions. An absence of key mRNA decay factors from EGP-bodies points toward an mRNA storage function for these bodies. Overall, this study highlights new potential control points in both the regulation of mRNA fate and the global control of translation initiation.</jats:p>",
  "DOI": "10.1083/jcb.200707010",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        10,
        2
      ]
    ],
    "date-time": "2007-10-02T00:26:49Z",
    "timestamp": 1191284809000
  },
  "page": "65-74",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 211,
  "title": "Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies",
  "prefix": "10.1083",
  "volume": "179",
  "author": [
    {
      "given": "Nathaniel P.",
      "family": "Hoyle",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK"
        }
      ]
    },
    {
      "given": "Lydia M.",
      "family": "Castelli",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK"
        }
      ]
    },
    {
      "given": "Susan G.",
      "family": "Campbell",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK"
        }
      ]
    },
    {
      "given": "Leah E.A.",
      "family": "Holmes",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK"
        }
      ]
    },
    {
      "given": "Mark P.",
      "family": "Ashe",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2007,
        10,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072911400904900_BIB1",
      "doi-asserted-by": "crossref",
      "first-page": "1114",
      "DOI": "10.1093/emboj/16.5.1114",
      "volume": "16",
      "year": "1997",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072911400904900_BIB2",
      "doi-asserted-by": "crossref",
      "first-page": "803",
      "DOI": "10.1083/jcb.200512082",
      "volume": "172",
      "year": "2006",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072911400904900_BIB3",
      "doi-asserted-by": "crossref",
      "first-page": "717",
      "DOI": "10.1261/rna.2340405",
      "volume": "11",
      "year": "2005",
      "journal-title": "RNA."
    },
    {
      "key": "2023072911400904900_BIB4",
      "doi-asserted-by": "crossref",
      "first-page": "833",
      "DOI": "10.1091/mbc.11.3.833",
      "volume": "11",
      "year": "2000",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072911400904900_BIB5",
      "doi-asserted-by": "crossref",
      "first-page": "6464",
      "DOI": "10.1093/emboj/20.22.6464",
      "volume": "20",
      "year": "2001",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072911400904900_BIB6",
      "doi-asserted-by": "crossref",
      "first-page": "2592",
      "DOI": "10.1091/mbc.e06-12-1149",
      "volume": "18",
      "year": "2007",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072911400904900_BIB7",
      "doi-asserted-by": "crossref",
      "first-page": "486",
      "DOI": "10.1126/science.1115791",
      "volume": "310",
      "year": "2005",
      "journal-title": "Science."
    },
    {
      "key": "2023072911400904900_BIB8",
      "doi-asserted-by": "crossref",
      "first-page": "1737",
      "DOI": "10.1017/S1355838200001059",
      "volume": "6",
      "year": "2000",
      "journal-title": "RNA."
    },
    {
      "key": "2023072911400904900_BIB9",
      "year": "2000"
    },
    {
      "key": "2023072911400904900_BIB10",
      "doi-asserted-by": "crossref",
      "first-page": "925",
      "DOI": "10.1083/jcb.200503162",
      "volume": "170",
      "year": "2005",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072911400904900_BIB11",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "DOI": "10.1016/j.cell.2005.02.024",
      "volume": "121",
      "year": "2005",
      "journal-title": "Cell."
    },
    {
      "key": "2023072911400904900_BIB12",
      "doi-asserted-by": "crossref",
      "first-page": "31",
      "DOI": "10.1083/jcb.200309008",
      "volume": "165",
      "year": "2004",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072911400904900_BIB13",
      "doi-asserted-by": "crossref",
      "first-page": "913",
      "DOI": "10.1083/jcb.200504039",
      "volume": "170",
      "year": "2005",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072911400904900_BIB14",
      "doi-asserted-by": "crossref",
      "first-page": "3882",
      "DOI": "10.1002/j.1460-2075.1994.tb06699.x",
      "volume": "13",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072911400904900_BIB15",
      "doi-asserted-by": "crossref",
      "first-page": "407",
      "DOI": "10.1146/annurev.micro.59.031805.133833",
      "volume": "59",
      "year": "2005",
      "journal-title": "Annu. Rev. Microbiol."
    },
    {
      "key": "2023072911400904900_BIB16",
      "doi-asserted-by": "crossref",
      "first-page": "2998",
      "DOI": "10.1128/MCB.24.7.2998-3010.2004",
      "volume": "24",
      "year": "2004",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072911400904900_BIB17",
      "doi-asserted-by": "crossref",
      "first-page": "1075",
      "DOI": "10.1002/yea.1415",
      "volume": "23",
      "year": "2006",
      "journal-title": "Yeast."
    },
    {
      "key": "2023072911400904900_BIB18",
      "doi-asserted-by": "crossref",
      "first-page": "947",
      "DOI": "10.1002/yea.1142",
      "volume": "21",
      "year": "2004",
      "journal-title": "Yeast."
    },
    {
      "key": "2023072911400904900_BIB19",
      "doi-asserted-by": "crossref",
      "first-page": "113",
      "DOI": "10.1016/j.molcel.2006.11.028",
      "volume": "25",
      "year": "2007",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072911400904900_BIB20",
      "doi-asserted-by": "crossref",
      "first-page": "657",
      "DOI": "10.1146/annurev.biochem.73.030403.080419",
      "volume": "73",
      "year": "2004",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "2023072911400904900_BIB21",
      "doi-asserted-by": "crossref",
      "first-page": "963",
      "DOI": "10.1042/bst0300963",
      "volume": "30",
      "year": "2002",
      "journal-title": "Biochem. Soc. Trans."
    },
    {
      "key": "2023072911400904900_BIB22",
      "doi-asserted-by": "crossref",
      "first-page": "1431",
      "DOI": "10.1083/jcb.147.7.1431",
      "volume": "147",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072911400904900_BIB23",
      "doi-asserted-by": "crossref",
      "first-page": "871",
      "DOI": "10.1083/jcb.200502088",
      "volume": "169",
      "year": "2005",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072911400904900_BIB24",
      "doi-asserted-by": "crossref",
      "first-page": "1141",
      "DOI": "10.1016/j.cell.2007.05.016",
      "volume": "129",
      "year": "2007",
      "journal-title": "Cell."
    },
    {
      "key": "2023072911400904900_BIB25",
      "doi-asserted-by": "crossref",
      "first-page": "187",
      "DOI": "10.1016/S0074-7696(01)03007-8",
      "volume": "203",
      "year": "2001",
      "journal-title": "Int. Rev. Cytol."
    },
    {
      "key": "2023072911400904900_BIB26",
      "doi-asserted-by": "crossref",
      "first-page": "383",
      "DOI": "10.1016/S1097-2765(00)80282-8",
      "volume": "2",
      "year": "1998",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072911400904900_BIB27",
      "doi-asserted-by": "crossref",
      "first-page": "4347",
      "DOI": "10.1128/MCB.21.13.4347-4368.2001",
      "volume": "21",
      "year": "2001",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072911400904900_BIB28",
      "doi-asserted-by": "crossref",
      "first-page": "5557",
      "DOI": "10.1128/MCB.19.8.5557",
      "volume": "19",
      "year": "1999",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072911400904900_BIB29",
      "doi-asserted-by": "crossref",
      "first-page": "1166",
      "DOI": "10.1038/sj.emboj.7600116",
      "volume": "23",
      "year": "2004",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072911400904900_BIB30",
      "doi-asserted-by": "crossref",
      "first-page": "635",
      "DOI": "10.1016/j.molcel.2007.02.011",
      "volume": "25",
      "year": "2007",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072911400904900_BIB31",
      "doi-asserted-by": "crossref",
      "first-page": "477",
      "DOI": "10.1038/nature03205",
      "volume": "433",
      "year": "2005",
      "journal-title": "Nature."
    },
    {
      "key": "2023072911400904900_BIB32",
      "year": "2000"
    },
    {
      "key": "2023072911400904900_BIB33",
      "year": "2000"
    },
    {
      "key": "2023072911400904900_BIB34",
      "doi-asserted-by": "crossref",
      "first-page": "805",
      "DOI": "10.1126/science.1082320",
      "volume": "300",
      "year": "2003",
      "journal-title": "Science."
    },
    {
      "key": "2023072911400904900_BIB35",
      "doi-asserted-by": "crossref",
      "first-page": "1095",
      "DOI": "10.1016/j.cell.2006.04.037",
      "volume": "125",
      "year": "2006",
      "journal-title": "Cell."
    },
    {
      "key": "2023072911400904900_BIB36",
      "doi-asserted-by": "crossref",
      "first-page": "9340",
      "DOI": "10.1128/MCB.25.21.9340-9349.2005",
      "volume": "25",
      "year": "2005",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072911400904900_BIB37",
      "doi-asserted-by": "crossref",
      "first-page": "1558",
      "DOI": "10.1073/pnas.79.5.1558",
      "volume": "79",
      "year": "1982",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072911400904900_BIB38",
      "doi-asserted-by": "crossref",
      "first-page": "371",
      "DOI": "10.1261/rna.7258505",
      "volume": "11",
      "year": "2005",
      "journal-title": "RNA."
    },
    {
      "key": "2023072911400904900_BIB39",
      "doi-asserted-by": "crossref",
      "first-page": "531",
      "DOI": "10.1046/j.1365-2958.2002.03172.x",
      "volume": "46",
      "year": "2002",
      "journal-title": "Mol. Microbiol."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/179/1/65/1889231/jcb_200707010.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/179/1/65/1889231/jcb_200707010.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T11:41:32Z",
    "timestamp": 1690630892000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/179/1/65/34872/Stress-dependent-relocalization-of-translationally"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        10,
        1
      ]
    ]
  },
  "references-count": 39,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          2007,
          10,
          8
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.200707010",
  "relation": {},
  "ISSN": [
    "1540-8140",
    "0021-9525"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2007,
        10,
        1
      ]
    ]
  }
}