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Nucleic Acids Res. 1998 September 1; 26(17): 3871–3876.
PMCID: PMC147800

The plurifunctional nucleolus.

Abstract

The nucleolus of eukaryotic cells was first described in the early 19th century and was discovered in the 1960s to be the seat of ribosome synthesis. Although rRNA transcription, rRNA processing and ribosome assembly have been clearly established as major functions of the nucleolus, recent studies suggest that the nucleolus participates in many other aspects of gene expression as well. Thus, the nucleolus has been implicated in the processing or nuclear export of certain mRNAs. In addition, new results indicate that biosyntheses of signal recognition particle RNA and telomerase RNA involve a nucleolar stage and that the nucleolus is also involved in processing of U6 RNA, one of the spliceosomal small nuclear RNAs. Interestingly, these three nucleolus-associated small nuclear RNAs (signal recognition particle RNA, telomerase RNA and U6 RNA) are components of catalytic ribonucleoprotein machines. Finally, recent work has also suggested that some transfer RNA precursors are processed in the nucleolus. The nucleolus may have evolutionarily descended from a proto-eukaryotic minimal genome that was spatially linked to vicinal RNA processing and ribonucleoprotein assembly events involved in gene read-out. The nucleolus of today's eukaryotes, now surrounded by the chromatin of over 2 billion years of genome expansion, may still perform these ancient functions, in addition to ribosome biosynthesis. The plurifunctional nucleolus concept has a strong footing in contemporary data and adds a new perspective to our current picture of the spatial-functional design of the cell nucleus.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • PERRY RP. On the nucleolar and nuclear dependence of cytoplasmic RNA synthesis in HeLa cells. Exp Cell Res. 1960 Jun;20:216–220. [PubMed]
  • PERRY RP, ERRERA M. The role of the nucleolus in ribonucleic acid-and protein synthesis. I. Incorporation of cytidine into normal and nucleolar inactivated HeLa cells. Biochim Biophys Acta. 1961 Apr 29;49:47–57. [PubMed]
  • EDSTROM JE, GRAMPP W, SCHOR N. The intracellular distribution and heterogeneity of ribonucleic acid in starfish oocytes. J Biophys Biochem Cytol. 1961 Dec;11:549–557. [PMC free article] [PubMed]
  • Perry RP. THE CELLULAR SITES OF SYNTHESIS OF RIBOSOMAL AND 4S RNA. Proc Natl Acad Sci U S A. 1962 Dec;48(12):2179–2186. [PubMed]
  • EDSTROEM JE, GALL JG. THE BASE COMPOSITION OF RIBONUCLEIC ACID IN LAMPBRUSH CHROMOSOMES, NUCLEOLI, NUCLEAR SAP, AND CYTOPLASM OF TRITURUS OOCYTES. J Cell Biol. 1963 Nov;19:279–284. [PMC free article] [PubMed]
  • BROWN DD, GURDON JB. ABSENCE OF RIBOSOMAL RNA SYNTHESIS IN THE ANUCLEOLATE MUTANT OF XENOPUS LAEVIS. Proc Natl Acad Sci U S A. 1964 Jan;51:139–146. [PubMed]
  • Penman S, Smith I, Holtzman E, Greenberg H. RNA metabolism in the HeLa cell nucleus and nucleolus. Natl Cancer Inst Monogr. 1966 Dec;23:489–512. [PubMed]
  • Miller OL, Jr, Beatty BR. Visualization of nucleolar genes. Science. 1969 May 23;164(3882):955–957. [PubMed]
  • HARRIS H, WATKINS JF. HYBRID CELLS DERIVED FROM MOUSE AND MAN: ARTIFICIAL HETEROKARYONS OF MAMMALIAN CELLS FROM DIFFERENT SPECIES. Nature. 1965 Feb 13;205:640–646. [PubMed]
  • Harris H. Behaviour of differentiated nuclei in heterokaryons of animal cells from different species. Nature. 1965 May 8;206(984):583–588. [PubMed]
  • Harris H. The reactivation of the red cell nucleus. J Cell Sci. 1967 Mar;2(1):23–32. [PubMed]
  • Bond VC, Wold B. Nucleolar localization of myc transcripts. Mol Cell Biol. 1993 Jun;13(6):3221–3230. [PMC free article] [PubMed]
  • Siomi H, Shida H, Nam SH, Nosaka T, Maki M, Hatanaka M. Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell. 1988 Oct 21;55(2):197–209. [PubMed]
  • Cullen BR, Hauber J, Campbell K, Sodroski JG, Haseltine WA, Rosen CA. Subcellular localization of the human immunodeficiency virus trans-acting art gene product. J Virol. 1988 Jul;62(7):2498–2501. [PMC free article] [PubMed]
  • Kubota S, Siomi H, Satoh T, Endo S, Maki M, Hatanaka M. Functional similarity of HIV-I rev and HTLV-I rex proteins: identification of a new nucleolar-targeting signal in rev protein. Biochem Biophys Res Commun. 1989 Aug 15;162(3):963–970. [PubMed]
  • Kadowaki T, Chen S, Hitomi M, Jacobs E, Kumagai C, Liang S, Schneiter R, Singleton D, Wisniewska J, Tartakoff AM. Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants. J Cell Biol. 1994 Aug;126(3):649–659. [PMC free article] [PubMed]
  • Kadowaki T, Hitomi M, Chen S, Tartakoff AM. Nuclear mRNA accumulation causes nucleolar fragmentation in yeast mtr2 mutant. Mol Biol Cell. 1994 Nov;5(11):1253–1263. [PMC free article] [PubMed]
  • Schneiter R, Kadowaki T, Tartakoff AM. mRNA transport in yeast: time to reinvestigate the functions of the nucleolus. Mol Biol Cell. 1995 Apr;6(4):357–370. [PMC free article] [PubMed]
  • Tani T, Derby RJ, Hiraoka Y, Spector DL. Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport. Mol Biol Cell. 1995 Nov;6(11):1515–1534. [PMC free article] [PubMed]
  • Potashkin JA, Derby RJ, Spector DL. Differential distribution of factors involved in pre-mRNA processing in the yeast cell nucleus. Mol Cell Biol. 1990 Jul;10(7):3524–3534. [PMC free article] [PubMed]
  • Spector DL. Macromolecular domains within the cell nucleus. Annu Rev Cell Biol. 1993;9:265–315. [PubMed]
  • Lamond AI, Carmo-Fonseca M. The coiled body. Trends Cell Biol. 1993 Jun;3(6):198–204. [PubMed]
  • Malatesta M, Zancanaro C, Martin TE, Chan EK, Amalric F, Lührmann R, Vogel P, Fakan S. Is the coiled body involved in nucleolar functions? Exp Cell Res. 1994 Apr;211(2):415–419. [PubMed]
  • Gall JG, Tsvetkov A, Wu Z, Murphy C. Is the sphere organelle/coiled body a universal nuclear component? Dev Genet. 1995;16(1):25–35. [PubMed]
  • Bell P, Dabauvalle MC, Scheer U. In vitro assembly of prenucleolar bodies in Xenopus egg extract. J Cell Biol. 1992 Sep;118(6):1297–1304. [PMC free article] [PubMed]
  • Raska I, Andrade LE, Ochs RL, Chan EK, Chang CM, Roos G, Tan EM. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp Cell Res. 1991 Jul;195(1):27–37. [PubMed]
  • Andrade LE, Chan EK, Raska I, Peebles CL, Roos G, Tan EM. Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med. 1991 Jun 1;173(6):1407–1419. [PMC free article] [PubMed]
  • Alliegro MC, Alliegro MA. Identification of a new coiled body component. Exp Cell Res. 1996 Sep 15;227(2):386–390. [PubMed]
  • Bohmann K, Ferreira JA, Lamond AI. Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus. J Cell Biol. 1995 Nov;131(4):817–831. [PMC free article] [PubMed]
  • Lyon CE, Bohmann K, Sleeman J, Lamond AI. Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus. Exp Cell Res. 1997 Jan 10;230(1):84–93. [PubMed]
  • Ghetti A, Piñol-Roma S, Michael WM, Morandi C, Dreyfuss G. hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res. 1992 Jul 25;20(14):3671–3678. [PMC free article] [PubMed]
  • Matera AG, Frey MR, Margelot K, Wolin SL. A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I. J Cell Biol. 1995 Jun;129(5):1181–1193. [PMC free article] [PubMed]
  • Walter P, Johnson AE. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu Rev Cell Biol. 1994;10:87–119. [PubMed]
  • Walter P, Blobel G. Purification of a membrane-associated protein complex required for protein translocation across the endoplasmic reticulum. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7112–7116. [PubMed]
  • Walter P, Blobel G. Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature. 1982 Oct 21;299(5885):691–698. [PubMed]
  • Jacobson MR, Pederson T. Localization of signal recognition particle RNA in the nucleolus of mammalian cells. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):7981–7986. [PubMed]
  • Dang CV, Lee WM. Nuclear and nucleolar targeting sequences of c-erb-A, c-myb, N-myc, p53, HSP70, and HIV tat proteins. J Biol Chem. 1989 Oct 25;264(30):18019–18023. [PubMed]
  • Reddy R, Li WY, Henning D, Choi YC, Nohga K, Busch H. Characterization and subcellular localization of 7-8 S RNAs of Novikoff hepatoma. J Biol Chem. 1981 Aug 25;256(16):8452–8457. [PubMed]
  • Ogg SC, Walter P. SRP samples nascent chains for the presence of signal sequences by interacting with ribosomes at a discrete step during translation elongation. Cell. 1995 Jun 30;81(7):1075–1084. [PubMed]
  • Fang G, Cech TR. Telomerase RNA localized in the replication band and spherical subnuclear organelles in hypotrichous ciliates. J Cell Biol. 1995 Jul;130(2):243–253. [PMC free article] [PubMed]
  • Haber JE, George JP. A mutation that permits the expression of normally silent copies of mating-type information in Saccharomyces cerevisiae. Genetics. 1979 Sep;93(1):13–35. [PubMed]
  • Klar AJ, Fogel S, Macleod K. MAR1-a Regulator of the HMa and HMalpha Loci in SACCHAROMYCES CEREVISIAE. Genetics. 1979 Sep;93(1):37–50. [PubMed]
  • Kennedy BK, Austriaco NR, Jr, Zhang J, Guarente L. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell. 1995 Feb 10;80(3):485–496. [PubMed]
  • Kennedy BK, Gotta M, Sinclair DA, Mills K, McNabb DS, Murthy M, Pak SM, Laroche T, Gasser SM, Guarente L. Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S. cerevisiae. Cell. 1997 May 2;89(3):381–391. [PubMed]
  • Sinclair DA, Guarente L. Extrachromosomal rDNA circles--a cause of aging in yeast. Cell. 1997 Dec 26;91(7):1033–1042. [PubMed]
  • Sinclair DA, Mills K, Guarente L. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science. 1997 Aug 29;277(5330):1313–1316. [PubMed]
  • Carmo-Fonseca M, Tollervey D, Pepperkok R, Barabino SM, Merdes A, Brunner C, Zamore PD, Green MR, Hurt E, Lamond AI. Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery. EMBO J. 1991 Jan;10(1):195–206. [PubMed]
  • Matera AG, Ward DC. Nucleoplasmic organization of small nuclear ribonucleoproteins in cultured human cells. J Cell Biol. 1993 May;121(4):715–727. [PMC free article] [PubMed]
  • Crain PF, McCloskey JA. The RNA modification database. Nucleic Acids Res. 1996 Jan 1;24(1):98–99. [PMC free article] [PubMed]
  • Jacobson MR, Cao LG, Taneja K, Singer RH, Wang YL, Pederson T. Nuclear domains of the RNA subunit of RNase P. J Cell Sci. 1997 Apr;110(Pt 7):829–837. [PubMed]
  • Jacobson MR, Cao LG, Wang YL, Pederson T. Dynamic localization of RNase MRP RNA in the nucleolus observed by fluorescent RNA cytochemistry in living cells. J Cell Biol. 1995 Dec;131(6 Pt 2):1649–1658. [PMC free article] [PubMed]
  • Petfalski E, Dandekar T, Henry Y, Tollervey D. Processing of the precursors to small nucleolar RNAs and rRNAs requires common components. Mol Cell Biol. 1998 Mar;18(3):1181–1189. [PMC free article] [PubMed]
  • ELSDALE TR, FISCHBERG M, SMITH S. A mutation that reduces nucleolar number in Xenopus laevis. Exp Cell Res. 1958 Jun;14(3):642–643. [PubMed]
  • Karpen GH, Schaefer JE, Laird CD. A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev. 1988 Dec;2(12B):1745–1763. [PubMed]
  • Oakes M, Nogi Y, Clark MW, Nomura M. Structural alterations of the nucleolus in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Mol Cell Biol. 1993 Apr;13(4):2441–2455. [PMC free article] [PubMed]
  • Nierras CR, Liebman SW, Warner JR. Does Saccharomyces need an organized nucleolus? Chromosoma. 1997 Jun;105(7-8):444–451. [PubMed]
  • Goessens G. Nucleolar structure. Int Rev Cytol. 1984;87:107–158. [PubMed]
  • Pederson T. Gene activation in eukaryotes: are nuclear acidic proteins the cause or the effect? Proc Natl Acad Sci U S A. 1974 Mar;71(3):617–621. [PubMed]
  • Politz JC, Browne ES, Wolf DE, Pederson T. Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6043–6048. [PubMed]
  • Pederson T. Thinking about a nuclear matrix. J Mol Biol. 1998 Mar 27;277(2):147–159. [PubMed]

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