DOI: 10.1091/mbc.e02-05-0271. Functional Proteomic Analysis of Human Nucleolus

Functional Proteomic Analysis of Human Nucleolus

10.1091/mbc.e02-05-0271

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

The notion of a “plurifunctional” nucleolus is now well established. However, molecular mechanisms underlying the biological processes occurring within this nuclear domain remain only partially understood. As a first step in elucidating these mechanisms we have carried out a proteomic analysis to draw up a list of proteins present within nucleoli of HeLa cells. This analysis allowed the identification of 213 different nucleolar proteins. This catalog complements that of the 271 proteins obtained recently by others, giving a total of ∼350 different nucleolar proteins. Functional classification of these proteins allowed outlining several biological processes taking place within nucleoli. Bioinformatic analyses permitted the assignment of hypothetical functions for 43 proteins for which no functional information is available. Notably, a role in ribosome biogenesis was proposed for 31 proteins. More generally, this functional classification reinforces the plurifunctional nature of nucleoli and provides convincing evidence that nucleoli may play a central role in the control of gene expression. Finally, this analysis supports the recent demonstration of a coupling of transcription and translation in higher eukaryotes.

Bibliography

Scherl, A., CoutÃ©, Y., DÃ©on, C., CallÃ©, A., Kindbeiter, K., Sanchez, J.-C., Greco, A., Hochstrasser, D., & Diaz, J.-J. (2002). Functional Proteomic Analysis of Human Nucleolus. Molecular Biology of the Cell, 13(11), 4100â4109.

Authors 9

Alexander Scherl (first)
Yohann Couté (additional)
Catherine Déon (additional)
Aleth Callé (additional)
Karine Kindbeiter (additional)
Jean-Charles Sanchez (additional)
Anna Greco (additional)
Denis Hochstrasser (additional)
Jean-Jacques Diaz (additional)

References 54 Referenced 397

10.1083/jcb.151.5.F23 / J. Cell Biol. by Aitchison J.D. (2000)
10.1096/fasebj.9.5.7896000 / FASEB J. by Allende J.E. (1995)
10.1016/S0960-9822(01)00650-9 / Curr. Biol. by Andersen J.S. (2002)
10.1016/S0955-0674(99)80041-6 / Curr. Opin. Cell Biol. by Belmont A.S. (1999)
10.1016/S0165-0270(01)00395-8 / J. Neurosci. Methods by Bergquist J. (2001)
10.1101/gad.12.16.2463 / Genes Dev. by Bertrand E. (1998)
10.1128/MCB.13.6.3221 / Mol Cell. Biol. by Bond V.C. (1993)
10.1016/0003-2697(76)90527-3 / Anal. Biochem. by Bradford M.M. (1976)
10.1111/j.1432-1033.1982.tb06989.x / Eur. J. Biochem. by Bugler B. (1982)
10.1017/S1355838299990064 / RNA by Buonomo S.B. (1999)
10.1083/jcb.153.1.169 / J. Cell Biol. by Chen D. (2001)
10.1016/S0960-9822(01)00328-1 / Curr. Biol. by d'Adda di Fagagna F. (2001)
10.1099/0022-1317-74-3-397 / J. Gen. Virol. by Diaz J.-J. (1993)
10.1016/S1357-2725(01)00046-2 / Int. J. Biochem. Cell. Biol. by Donato R. (2001)
10.1042/bj3560297 / Biochem. J. by Dundr M. (2001)
10.1093/nar/26.7.1551 / Nucleic Acids Res. by Dynan W.S. (1998)
10.1016/S0921-8777(99)00006-3 / Mutat. Res. by Featherstone C. (1999)
10.1016/0042-6822(57)90038-7 / Virology by Fraenkel-Conrat H. (1957)
10.1002/(SICI)1097-4644(19981201)71:3<363::AID-JCB5>3.0.CO;2-W / J. Cell Biochem. by Gerner C. (1998)
10.1126/science.271.5255.1513 / Science by Görlich D. (1996)
10.1002/(SICI)1522-2683(19991201)20:18<3535::AID-ELPS3535>3.0.CO;2-J / Electrophoresis by Gras R. (1999)
10.1016/S0092-8674(00)80542-5 / Cell by Hentze M.W. (1999)
10.1126/science.1061216 / Science by Iborra F.J. (2001)
10.1016/S0955-0674(98)80008-2 / Curr. Opin. Cell Biol. by Johnson F.B. (1998)
10.1002/1522-2683(20001001)21:16<3483::AID-ELPS3483>3.0.CO;2-X / Electrophoresis by Jung E. (2000)
10.1083/jcb.126.3.649 / J. Cell Biol. by Kadowaki T. (1994)
10.1091/mbc.5.11.1253
{'key': 'B28', 'first-page': '389', 'volume': '3', 'author': 'Kalland K.H.', 'year': '1991', 'journal-title': 'New Biol.'} / New Biol. by Kalland K.H. (1991)
10.1016/S0962-8924(01)02144-4 / Trends Cell Biol. by Kuersten S. (2001)
10.1038/227680a0 / Nature by Laemmli U.K. (1970)
10.1016/S0014-5793(01)03143-X / FEBS Lett. by Leary D.J. (2001)
10.1083/jcb.122.5.1079 / J. Cell Biol. by Lenormand P. (1993)
10.1126/science.288.5470.1385 / Science by Lewis J.D. (2000)
10.1007/BF00269998 / Mol. Gen. Genet. by Madjar J.-J. (1979)
10.1016/0003-2697(79)90641-9 / Anal. Biochem. by Madjar J.-J. (1979)
10.1016/S0962-8924(99)01606-2 / Trends Cell Biol. by Matera A.G. (1999)
10.1016/0955-0674(95)80085-9 / Curr. Opin. Cell Biol. by Melese T. (1995)
10.1083/jcb.200108110 / J. Cell Biol. by Misteli T. (2001)
10.1016/S0091-679X(08)61142-5 / Methods Cell Biol. by Muramatsu M. (1978)
10.1016/S0091-679X(08)60884-5 / Methods Cell Biol. by Ochs R.L. (1998)
10.1016/S0962-8924(00)01738-4 / Trends Cell Biol. by Olson M.O. (2000)
10.1093/nar/26.17.3871 / Nucleic Acids Res. by Pederson T. (1998)
10.1083/jcb.148.6.1091 / J. Cell Biol. by Pederson T. (2000)
10.1038/35007077 / Nature by Phair R.D. (2000)
10.1016/S1097-2765(01)00347-1 / Mol. Cell by Pickart C.M. (2001)
10.1073/pnas.97.1.55 / Proc. Natl. Acad. Sci. USA by Politz J.C. (2000)
10.1006/excr.1994.1283 / Exp. Cell Res. by Roussel P. (1994)
10.1016/S0955-0674(99)80054-4 / Curr. Opin. Cell Biol. by Scheer U. (1999)
{'key': 'B49', 'first-page': '27', 'volume': '1552', 'author': 'Tong W.M.', 'year': '2001', 'journal-title': 'Biochim. Biophys. Acta'} / Biochim. Biophys. Acta by Tong W.M. (2001)
10.1242/jcs.80.1.103 / J. Cell Sci. by Verheijen R. (1986)
10.1016/S0955-0674(00)00102-2 / Curr. Opin. Cell Biol. by Visintin R. (2000)
10.1073/pnas.47.1.18 / Proc. Natl. Acad. Sci. USA by Waller J.R. (1961)
10.1016/S0955-0674(99)80053-2 / Curr. Opin. Cell Biol. by Weinstein L.B. (1999)
10.1126/science.7754385 / Science by Weis K. (1995)

Dates

Type	When
Created	22 years, 9 months ago (Nov. 12, 2002, 2:42 p.m.)
Deposited	4 years, 2 months ago (May 30, 2021, 4:19 p.m.)
Indexed	3 weeks, 1 day ago (Aug. 6, 2025, 8:40 a.m.)
Issued	22 years, 9 months ago (Nov. 1, 2002)
Published	22 years, 9 months ago (Nov. 1, 2002)
Published Print	22 years, 9 months ago (Nov. 1, 2002)

Funders 0

None

BibTeX

@article{Scherl_2002, title={Functional Proteomic Analysis of Human Nucleolus}, volume={13}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e02-05-0271}, DOI={10.1091/mbc.e02-05-0271}, number={11}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Scherl, Alexander and Couté, Yohann and Déon, Catherine and Callé, Aleth and Kindbeiter, Karine and Sanchez, Jean-Charles and Greco, Anna and Hochstrasser, Denis and Diaz, Jean-Jacques}, editor={Gall, Joseph}, year={2002}, month=nov, pages={4100–4109} }

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      "first-page": "F23",
      "DOI": "10.1083/jcb.151.5.F23",
      "volume": "151",
      "author": "Aitchison J.D.",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B2",
      "doi-asserted-by": "crossref",
      "first-page": "313",
      "DOI": "10.1096/fasebj.9.5.7896000",
      "volume": "9",
      "author": "Allende J.E.",
      "year": "1995",
      "journal-title": "FASEB J."
    },
    {
      "key": "B3",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/S0960-9822(01)00650-9",
      "volume": "12",
      "author": "Andersen J.S.",
      "year": "2002",
      "journal-title": "Curr. Biol."
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    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "307",
      "DOI": "10.1016/S0955-0674(99)80041-6",
      "volume": "11",
      "author": "Belmont A.S.",
      "year": "1999",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "3",
      "DOI": "10.1016/S0165-0270(01)00395-8",
      "volume": "109",
      "author": "Bergquist J.",
      "year": "2001",
      "journal-title": "J. Neurosci. Methods"
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "2463",
      "DOI": "10.1101/gad.12.16.2463",
      "volume": "12",
      "author": "Bertrand E.",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "3221",
      "DOI": "10.1128/MCB.13.6.3221",
      "volume": "13",
      "author": "Bond V.C.",
      "year": "1993",
      "journal-title": "Mol Cell. Biol."
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "248",
      "DOI": "10.1016/0003-2697(76)90527-3",
      "volume": "72",
      "author": "Bradford M.M.",
      "year": "1976",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1111/j.1432-1033.1982.tb06989.x",
      "volume": "128",
      "author": "Bugler B.",
      "year": "1982",
      "journal-title": "Eur. J. Biochem."
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "993",
      "DOI": "10.1017/S1355838299990064",
      "volume": "5",
      "author": "Buonomo S.B.",
      "year": "1999",
      "journal-title": "RNA"
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "169",
      "DOI": "10.1083/jcb.153.1.169",
      "volume": "153",
      "author": "Chen D.",
      "year": "2001",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "1192",
      "DOI": "10.1016/S0960-9822(01)00328-1",
      "volume": "11",
      "author": "d'Adda di Fagagna F.",
      "year": "2001",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "397",
      "DOI": "10.1099/0022-1317-74-3-397",
      "volume": "74",
      "author": "Diaz J.-J.",
      "year": "1993",
      "journal-title": "J. Gen. Virol."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "637",
      "DOI": "10.1016/S1357-2725(01)00046-2",
      "volume": "33",
      "author": "Donato R.",
      "year": "2001",
      "journal-title": "Int. J. Biochem. Cell. Biol."
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "297",
      "DOI": "10.1042/bj3560297",
      "volume": "356",
      "author": "Dundr M.",
      "year": "2001",
      "journal-title": "Biochem. J."
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "1551",
      "DOI": "10.1093/nar/26.7.1551",
      "volume": "26",
      "author": "Dynan W.S.",
      "year": "1998",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "3",
      "DOI": "10.1016/S0921-8777(99)00006-3",
      "volume": "434",
      "author": "Featherstone C.",
      "year": "1999",
      "journal-title": "Mutat. Res."
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0042-6822(57)90038-7",
      "volume": "4",
      "author": "Fraenkel-Conrat H.",
      "year": "1957",
      "journal-title": "Virology"
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "363",
      "DOI": "10.1002/(SICI)1097-4644(19981201)71:3<363::AID-JCB5>3.0.CO;2-W",
      "volume": "71",
      "author": "Gerner C.",
      "year": "1998",
      "journal-title": "J. Cell Biochem."
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "1513",
      "DOI": "10.1126/science.271.5255.1513",
      "volume": "271",
      "author": "G\u00f6rlich D.",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "3535",
      "DOI": "10.1002/(SICI)1522-2683(19991201)20:18<3535::AID-ELPS3535>3.0.CO;2-J",
      "volume": "20",
      "author": "Gras R.",
      "year": "1999",
      "journal-title": "Electrophoresis"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "307",
      "DOI": "10.1016/S0092-8674(00)80542-5",
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      "author": "Hentze M.W.",
      "year": "1999",
      "journal-title": "Cell"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "1139",
      "DOI": "10.1126/science.1061216",
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      "year": "2001",
      "journal-title": "Science"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "332",
      "DOI": "10.1016/S0955-0674(98)80008-2",
      "volume": "10",
      "author": "Johnson F.B.",
      "year": "1998",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "3483",
      "DOI": "10.1002/1522-2683(20001001)21:16<3483::AID-ELPS3483>3.0.CO;2-X",
      "volume": "21",
      "author": "Jung E.",
      "year": "2000",
      "journal-title": "Electrophoresis"
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "649",
      "DOI": "10.1083/jcb.126.3.649",
      "volume": "126",
      "author": "Kadowaki T.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.5.11.1253"
    },
    {
      "key": "B28",
      "first-page": "389",
      "volume": "3",
      "author": "Kalland K.H.",
      "year": "1991",
      "journal-title": "New Biol."
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1016/S0962-8924(01)02144-4",
      "volume": "11",
      "author": "Kuersten S.",
      "year": "2001",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "680",
      "DOI": "10.1038/227680a0",
      "volume": "227",
      "author": "Laemmli U.K.",
      "year": "1970",
      "journal-title": "Nature"
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "145",
      "DOI": "10.1016/S0014-5793(01)03143-X",
      "volume": "509",
      "author": "Leary D.J.",
      "year": "2001",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "1079",
      "DOI": "10.1083/jcb.122.5.1079",
      "volume": "122",
      "author": "Lenormand P.",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "1385",
      "DOI": "10.1126/science.288.5470.1385",
      "volume": "288",
      "author": "Lewis J.D.",
      "year": "2000",
      "journal-title": "Science"
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.1007/BF00269998",
      "volume": "171",
      "author": "Madjar J.-J.",
      "year": "1979",
      "journal-title": "Mol. Gen. Genet."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "174",
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