DOI: 10.1091/mbc.e10-02-0099. Defects in the Secretory Pathway and High Ca<sup>2+</sup>Induce Multiple P-bodies

Defects in the Secretory Pathway and High Ca2+Induce Multiple P-bodies

10.1091/mbc.e10-02-0099

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

mRNA is sequestered and turned over in cytoplasmic processing bodies (PBs), which are induced by various cellular stresses. Unexpectedly, in Saccharomyces cerevisiae, mutants of the small GTPase Arf1 and various secretory pathway mutants induced a significant increase in PB number, compared with PB induction by starvation or oxidative stress. Exposure of wild-type cells to osmotic stress or high extracellular Ca2+mimicked this increase in PB number. Conversely, intracellular Ca2+-depletion strongly reduced PB formation in the secretory mutants. In contrast to PB induction through starvation or osmotic stress, PB formation in secretory mutants and by Ca2+required the PB components Pat1 and Scd6, and calmodulin, indicating that different stressors act through distinct pathways. Consistent with this hypothesis, when stresses were combined, PB number did not correlate with the strength of the translational block, but rather with the type of stress encountered. Interestingly, independent of the stressor, PBs appear as spheres of ∼40–100 nm connected to the endoplasmic reticulum (ER), consistent with the idea that translation and silencing/degradation occur in a spatially coordinated manner at the ER. We propose that PB assembly in response to stress occurs at the ER and depends on intracellular signals that regulate PB number.

Bibliography

Kilchert, C., Weidner, J., Prescianotto-Baschong, C., & Spang, A. (2010). Defects in the Secretory Pathway and High Ca2+Induce Multiple P-bodies. Molecular Biology of the Cell, 21(15), 2624â2638.

Authors 4

Cornelia Kilchert (first)
Julie Weidner (additional)
Cristina Prescianotto-Baschong (additional)
Anne Spang (additional)

References 60 Referenced 54

10.1091/mbc.e08-05-0513
10.1261/rna.144606 / RNA by Anderson J. R. (2006)
10.1261/rna.2340405 / RNA by Andrei M. A. (2005)
10.1074/jbc.M402068200 / J. Biol. Chem by Aronov S. (2004)
10.1091/mbc.11.3.833
10.1074/jbc.271.38.23357 / J. Biol. Chem by Batiza A. F. (1996)
10.1073/pnas.0703805104 / Proc. Natl. Acad. Sci. USA by Bi J. (2007)
10.1093/emboj/19.7.1661 / EMBO J by Bouveret E. (2000)
10.1083/jcb.200807043 / J. Cell Biol by Buchan J. R. (2008)
10.1261/rna.502507 / RNA by Chowdhury A. (2007)
10.1016/j.cell.2005.07.012 / Cell by Coller J. (2005)
10.1016/S0092-8674(00)81360-4 / Cell by Cox J. S. (1996)
10.1007/s00294-007-0151-0 / Curr. Genet by De Filippi L. (2007)
10.1073/pnas.94.10.5201 / Proc. Natl. Acad. Sci. USA by de la Cruz J. (1997)
10.1083/jcb.200601153 / J. Cell Biol by Decker C. J. (2006)
10.1083/jcb.200704147 / J. Cell Biol by Decker C. J. (2007)
10.1016/S1097-2765(04)00008-5 / Mol. Cell by Deloche O. (2004)
10.1093/emboj/18.19.5411 / EMBO J by Dunckley T. (1999)
10.1101/gr.7.12.1174 / Genome Res by Erdeniz N. (1997)
10.1128/MCB.00128-07 / Mol. Cell. Biol by Eulalio A. (2007)
10.1083/jcb.200504039 / J. Cell Biol by Ferraiuolo M. A. (2005)
10.1016/j.molcel.2008.11.001 / Mol. Cell by Franks T. M. (2008)
10.1016/0092-8674(91)90547-C / Cell by Geiser J. R. (1991)
10.1242/jcs.045104 / J. Cell Sci by Grousl T. (2009)
10.1093/nar/30.6.e23 / Nucleic Acids Res by Gueldener U. (2002)
10.1093/jb/mvj089 / J. Biochem by Hayashi M. (2006)
10.1128/EC.3.3.695-704.2004 / Eukaryot. Cell by Heath V. L. (2004)
10.1128/MMBR.66.2.300-372.2002 / Microbiol. Mol. Biol. Rev by Hohmann S. (2002)
10.1083/jcb.200707010 / J. Cell Biol by Hoyle N. P. (2007)
10.1083/jcb.200502088 / J. Cell Biol by Kedersha N. (2005)
10.1111/j.1365-2443.2005.00921.x / Genes Cells by Kimata Y. (2006)
10.1002/(SICI)1097-0061(199907)15:10B<963::AID-YEA399>3.0.CO;2-W / Yeast by Knop M. (1999)
10.1128/MCB.13.5.3067 / Mol. Cell. Biol by Lee K. S. (1993)
10.1074/jbc.M205037200 / J. Biol. Chem by Matsumoto T. K. (2002)
10.1128/MCB.13.1.521 / Mol. Cell. Biol by Nelson K. K. (1993)
10.1126/science.8310294 / Science by Ohya Y. (1994)
10.1016/j.molcel.2007.02.011 / Mol. Cell by Parker R. (2007)
10.1371/journal.pbio.0020246 / PLoS Biol by Patil C. K. (2004)
10.1034/j.1600-0854.2002.30106.x / Traffic by Prescianotto-Baschong C. (2002)
10.1242/jcs.024976 / J. Cell Sci by Reijns M. A. (2008)
10.1261/rna.1435709 / RNA by Romero-Santacreu L. (2009)
10.1093/emboj/18.12.3451 / EMBO J by Salgado-Garrido J. (1999)
10.1128/MCB.22.5.1329-1339.2002 / Mol. Cell. Biol by Schmelzle T. (2002)
10.1016/j.cub.2006.06.025 / Curr. Biol by Schmid M. (2006)
10.1016/0076-6879(91)94004-V / Methods Enzymol by Sherman F. (1991)
10.1126/science.1082320 / Science by Sheth U. (2003)
10.1016/S0092-8674(00)80369-4 / Cell by Sidrauski C. (1997)
10.1093/genetics/122.1.19 / Genetics by Sikorski R. S. (1989)
10.1242/jcs.109.9.2229 / J. Cell Sci by Spang A. (1996)
10.1091/mbc.e05-09-0874
10.1371/journal.pone.0010006 / PLoS One by Swisher K.D. (2010)
10.1091/mbc.e07-03-0199
10.1261/rna.7258505 / RNA by Teixeira D. (2005)
10.1038/35006676 / Nature by Tharun S. (2000)
10.1534/genetics.104.034322 / Genetics by Tharun S. (2005)
10.1016/S1097-2765(01)00395-1 / Mol. Cell by Tharun S. (2001)
10.1091/mbc.e04-05-0411
10.1046/j.1365-2958.2000.02002.x / Mol. Microbiol by Van Wuytswinkel O. (2000)
10.1128/EC.4.9.1513-1525.2005 / Eukaryot. Cell by Wilczynska Z. (2005)
10.1016/j.devcel.2005.09.015 / Dev. Cell by Wilhelm J. E. (2005)

Dates

Type	When
Created	15 years, 2 months ago (June 2, 2010, 10:38 p.m.)
Deposited	3 years, 9 months ago (Oct. 28, 2021, 4:49 p.m.)
Indexed	4 months, 2 weeks ago (April 9, 2025, 7:24 p.m.)
Issued	15 years ago (Aug. 1, 2010)
Published	15 years ago (Aug. 1, 2010)
Published Print	15 years ago (Aug. 1, 2010)

Funders 0

None

BibTeX

@article{Kilchert_2010, title={Defects in the Secretory Pathway and High Ca2+Induce Multiple P-bodies}, volume={21}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e10-02-0099}, DOI={10.1091/mbc.e10-02-0099}, number={15}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Kilchert, Cornelia and Weidner, Julie and Prescianotto-Baschong, Cristina and Spang, Anne}, editor={Gilmore, Reid}, year={2010}, month=aug, pages={2624–2638} }

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      "first-page": "13810",
      "DOI": "10.1073/pnas.0703805104",
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    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1093/emboj/19.7.1661",
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      "year": "2000",
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      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "441",
      "DOI": "10.1083/jcb.200807043",
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      "author": "Buchan J. R.",
      "year": "2008",
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    {
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      "doi-asserted-by": "crossref",
      "first-page": "998",
      "DOI": "10.1261/rna.502507",
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      "author": "Chowdhury A.",
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      "journal-title": "RNA"
    },
    {
      "key": "B11",
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      "first-page": "875",
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      "year": "2005",
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    {
      "key": "B12",
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      "author": "Cox J. S.",
      "year": "1996",
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    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "171",
      "DOI": "10.1007/s00294-007-0151-0",
      "volume": "52",
      "author": "De Filippi L.",
      "year": "2007",
      "journal-title": "Curr. Genet"
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      "first-page": "5201",
      "DOI": "10.1073/pnas.94.10.5201",
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      "journal-title": "Proc. Natl. Acad. Sci. USA"
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    {
      "key": "B15",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1083/jcb.200601153",
      "volume": "173",
      "author": "Decker C. J.",
      "year": "2006",
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    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "437",
      "DOI": "10.1083/jcb.200704147",
      "volume": "179",
      "author": "Decker C. J.",
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    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1016/S1097-2765(04)00008-5",
      "volume": "13",
      "author": "Deloche O.",
      "year": "2004",
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    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "5411",
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      "author": "Dunckley T.",
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    {
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      "year": "1997",
      "journal-title": "Genome Res"
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    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "3970",
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      "year": "2007",
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    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "913",
      "DOI": "10.1083/jcb.200504039",
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      "author": "Ferraiuolo M. A.",
      "year": "2005",
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    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "605",
      "DOI": "10.1016/j.molcel.2008.11.001",
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      "year": "2008",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B23",
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      "DOI": "10.1016/0092-8674(91)90547-C",
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      "author": "Geiser J. R.",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "2078",
      "DOI": "10.1242/jcs.045104",
      "volume": "122",
      "author": "Grousl T.",
      "year": "2009",
      "journal-title": "J. Cell Sci"
    },
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      "key": "B25",
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      "author": "Gueldener U.",
      "year": "2002",
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    },
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      "key": "B26",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1093/jb/mvj089",
      "volume": "139",
      "author": "Hayashi M.",
      "year": "2006",
      "journal-title": "J. Biochem"
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "695",
      "DOI": "10.1128/EC.3.3.695-704.2004",
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      "year": "2002",
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    },
    {
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      "DOI": "10.1083/jcb.200502088",
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      "author": "Kedersha N.",
      "year": "2005",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "59",
      "DOI": "10.1111/j.1365-2443.2005.00921.x",
      "volume": "11",
      "author": "Kimata Y.",
      "year": "2006",
      "journal-title": "Genes Cells"
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "963",
      "DOI": "10.1002/(SICI)1097-0061(199907)15:10B<963::AID-YEA399>3.0.CO;2-W",
      "volume": "15",
      "author": "Knop M.",
      "year": "1999",
      "journal-title": "Yeast"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "3067",
      "DOI": "10.1128/MCB.13.5.3067",
      "volume": "13",
      "author": "Lee K. S.",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "33075",
      "DOI": "10.1074/jbc.M205037200",
      "volume": "277",
      "author": "Matsumoto T. K.",
      "year": "2002",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "521",
      "DOI": "10.1128/MCB.13.1.521",
      "volume": "13",
      "author": "Nelson K. K.",
      "year": "1993",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "963",
      "DOI": "10.1126/science.8310294",
      "volume": "263",
      "author": "Ohya Y.",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "B37",
      "doi-asserted-by": "crossref",
      "first-page": "635",
      "DOI": "10.1016/j.molcel.2007.02.011",
      "volume": "25",
      "author": "Parker R.",
      "year": "2007",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B38",
      "doi-asserted-by": "crossref",
      "first-page": "E246",
      "DOI": "10.1371/journal.pbio.0020246",
      "volume": "2",
      "author": "Patil C. K.",
      "year": "2004",
      "journal-title": "PLoS Biol"
    },
    {
      "key": "B39",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1034/j.1600-0854.2002.30106.x",
      "volume": "3",
      "author": "Prescianotto-Baschong C.",
      "year": "2002",
      "journal-title": "Traffic"
    },
    {
      "key": "B40",
      "doi-asserted-by": "crossref",
      "first-page": "2463",
      "DOI": "10.1242/jcs.024976",
      "volume": "121",
      "author": "Reijns M. A.",
      "year": "2008",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "B41",
      "doi-asserted-by": "crossref",
      "first-page": "1110",
      "DOI": "10.1261/rna.1435709",
      "volume": "15",
      "author": "Romero-Santacreu L.",
      "year": "2009",
      "journal-title": "RNA"
    },
    {
      "key": "B42",
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