Advances in the study of the nucleolus

FENG Jin-Mei; SUN Jun; WEN Jian-Fan

doi:10.3724/SP.J.1141.2012.06549

Volume 33 Issue 6

Nov. 2012

Turn off MathJax

Article Contents

Article Navigation > Zoological Research > 2012 > 33(6): 549-556

FENG Jin-Mei, SUN Jun, WEN Jian-Fan. Advances in the study of the nucleolus. Zoological Research, 2012, 33(6): 549-556. doi: 10.3724/SP.J.1141.2012.06549

Citation:

FENG Jin-Mei, SUN Jun, WEN Jian-Fan. Advances in the study of the nucleolus. Zoological Research, 2012, 33(6): 549-556. doi: 10.3724/SP.J.1141.2012.06549

FENG Jin-Mei, SUN Jun, WEN Jian-Fan. Advances in the study of the nucleolus. Zoological Research, 2012, 33(6): 549-556. doi: 10.3724/SP.J.1141.2012.06549

Citation:

FENG Jin-Mei, SUN Jun, WEN Jian-Fan. Advances in the study of the nucleolus. Zoological Research, 2012, 33(6): 549-556. doi: 10.3724/SP.J.1141.2012.06549

PDF( 676 KB)

Advances in the study of the nucleolus

doi: 10.3724/SP.J.1141.2012.06549

State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, the Chinese Academy of Sciences, Kunming 650223, China

Received Date: 2012-09-06
Rev Recd Date: 2012-10-15
Publish Date: 2012-12-08

Abstract

Abstract

As the most prominent sub-nuclear compartment in the interphase nucleus and the site of ribosome biogenesis, the nucleolus synthesizes and processes rRNA and also assembles ribosomal subunits. Though several lines of research in recent years have indicated that the nucleolus might have additional functions—such as the assembling of signal recognition particles, the processing of mRNA, tRNA and telomerase activities, and regulating the cell cycle—proteomic analyses of the nucleolus in three representative eukaryotic species has shown that a plethora of proteins either have no association with ribosome biogenesis or are of presently unknown function. This phenomenon further indicates that the composition and function of the nucleolus is far more complicated than previously thought. Meanwhile, the available nucleolar proteome databases has provided new approaches and led to remarkable progress in understanding the nucleolus. Here, we have summarized recent advances in the study of the nucleolus, including new discoveries of its structure, function, genomics/proteomics as well as its origin and evolution. Moreover, we highlight several of the important unresolved issues in this field.
- Nucleolus,
- Structure,
- Function,
- Proteomics,
- Origin and evolution

FullText(HTML)

References(81)

References

[1]	Ahmad Y, Boisvert FM, Gregor P, Cobley A, Lamond AI. 2009. NOPdb: Nucleolar Proteome Database--2008 update [J]. Nucleic Acids Res, 37(Database issue): D181-D184.
[2]	Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, Lamond AI, Mann M. 2005. Nucleolar proteome dynamics [J]. Nature, 433(7021): 77-83.
[3]	Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Mann M, Lamond AI. 2002. Directed proteomic analysis of the human nucleolus [J]. Curr Biol, 12(1): 1-11.
[4]	Bergquist J, Gobom J, Blomberg A, Roepstorff P, Ekman R. 2001. Identification of nuclei associated proteins by 2D-gel electrophoresis and mass spectrometry [J]. J Neurosci Methods, 109(1): 3-11.
[5]	Bertrand E, Houser-Scott F, Kendall A, Singer RH, Engelke DR. 1998. Nucleolar localization of early tRNA processing [J]. Genes Dev, 12(16): 2463-2468.
[6]	Birnstiel ML, Hyde BB. 1963. Protein synthesis by isolated pea nucleoli [J]. J Cell Biol, 18(1): 41-50.
[7]	Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. 2007. The multifunctional nucleolus [J]. Nat Rev Mol Cell Biol, 8(7): 574-585.
[8]	Bond VC, Wold B. 1993. Nucleolar localization of myc transcripts [J]. Mol Cell Biol, 13(6): 3221-3230.
[9]	Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. 2010. The nucleolus under stress [J]. Mol Cell, 40(2): 216-227.
[10]	Brown JW, Shaw PJ. 2008. The role of the plant nucleolus in pre-mRNA processing [J]. Curr Top Microbiol Immunol, 326: 291-311.
[11]	Casafont I, Bengoechea R, Navascues J, Pena E, Berciano MT, Lafarga M. 2007. The giant fibrillar center: a nucleolar structure enriched in upstream binding factor (UBF) that appears in transcriptionally more active sensory ganglia neurons [J]. J Struct Biol, 159(3): 451-461.
[12]	Custódio N, Carvalho C, Condado I, Antoniou M, Blencowe BJ, Carmo- Fonseca M. 2004. In vivo recruitment of exon junction complex proteins to transcription sites in mammalian cell nuclei [J]. RNA, 10(4): 622-633.
[13]	Desterro JM, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M. 2003. Dynamic association of RNA-editing enzymes with the nucleolus [J]. J Cell Sci, 116(Pt 9): 1805-1818.
[14]	Etheridge KT, Banik SS, Armbruster BN, Zhu YS, Terns RM, Terns MP, Counter CM. 2002. The nucleolar localization domain of the catalytic subunit of human telomerase [J]. J Biol Chem, 277(27): 24764-24770.
[15]	Feng JM, Sun J, Xin DD, Wen JF. 2012. Comparative analysis of the 5S rRNA and its associated proteins reveals unique primitive rather than parasitic features in Giardia lamblia [J]. PLoS One, 7(6): e36878.
[16]	Figueiredo LM, Rocha EP, Mancio-Silva L, Prevost C, Hernandez-Verdun D, Scherf A. 2005. The unusually large Plasmodium telomerase reverse-transcriptase localizes in a discrete compartment associated with the nucleolus [J]. Nucleic Acids Res, 33(3): 1111-1122.
[17]	Gerbi SA, Lange TS. 2002. All small nuclear RNAs (snRNAs) of the [U4/U6. U5] Tri-snRNP localize to nucleoli; Identification of the nucleolar localization element of U6 snRNA [J]. Mol Biol Cell, 13(9): 3123-3137.
[18]	Grisendi S, Bernardi R, Rossi M, Cheng K, Khandker L, Manova K, Pandolfi PP. 2005. Role of nucleophosmin in embryonic development and tumorigenesis [J]. Nature, 437(7055): 147-153.
[19]	Grosshans H, Deinert K, Hurt E, Simos G. 2001. Biogenesis of the signal recognition particle (SRP) involves import of SRP proteins into the nucleolus, assembly with the SRP-RNA, and Xpo1p-mediated export [J]. J Cell Biol, 153(4): 745-762.
[20]	Guarente L. 1997. Link between aging and the nucleolus [J]. Genes Dev, 11(19): 2449-2455.
[21]	Guo J, Chen YH, Zhou KY, Li JY. 2005. Distribution of rDNA in the nucleus of Giardia lamblia - Detection by Ag-I silver stain [J]. Anal Quant Cytol Histol, 27(2): 79-82.
[22]	Handwerger KE, Cordero JA, Gall JG. 2005. Cajal bodies, nucleoli, and speckles in the Xenopus oocyte nucleus have a low-density, sponge-like structure [J]. Mol Biol Cell, 16(1): 202-211.
[23]	Harris H. 1967. The reactivation of the red cell nucleus [J]. J Cell Sci, 2(1): 23-32.
[24]	Hetman M, Pietrzak M. 2012. Emerging roles of the neuronal nucleolus [J]. Trends Neurosci, 35(5): 305-314.
[25]	Hozak P, Cook PR, Schofer C, Mosgoller W, Wachtler F. 1994. Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells [J]. J Cell Sci, 107( Pt 2): 639-648.
[26]	Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. 2003. Global analysis of protein localization in budding yeast [J]. Nature, 425(6959): 686-691.
[27]	Iborra FJ, Jackson DA, Cook PR. 2001. Coupled transcription and translation within nuclei of mammalian cells [J]. Science, 293(5532): 1139-1142.
[28]	Jacobson MR, Pederson T. 1998. Localization of signal recognition particle RNA in the nucleolus of mammalian cells [J]. Proc Natl Acad Sci U S A, 95(14): 7981-7986.
[29]	Jacobson MR, Cao LG, Taneja K, Singer RH, Wang YL, Pederson T. 1997. Nuclear domains of the RNA subunit of RNase P [J]. J Cell Sci, 110( Pt 7): 829-837.
[30]	Jady BE, Bertrand E, Kiss T. 2004. Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal [J]. J Cell Biol, 164(5): 647-652.
[31]	Jady BE, Darzacq X, Tucker KE, Matera AG, Bertrand E, Kiss T. 2003. Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm [J]. EMBO J, 22(8): 1878-1888.
[32]	Jarrous N, Wolenski JS, Wesolowski D, Lee C, Altman S. 1999. Localization in the nucleolus and coiled bodies of protein subunits of the ribonucleoprotein ribonuclease P [J]. J Cell Biol, 146(3): 559-572.
[33]	Jimenez-Garcia LF, Zavala G, Chavez-Munguia B, Ramos-Godinez Mdel P, Lopez-Velazquez G, Segura-Valdez Mde L, Montanez C, Hehl AB, Arguello-Garcia R, Ortega-Pierres G. 2008. Identification of nucleoli in the early branching protist Giardia duodenalis [J]. Int J Parasitol, 38(11): 1297-1304.
[34]	Jung E, Hoogland C, Chiappe D, Sanchez JC, Hochstrasser DF. 2000. The establishment of a human liver nuclei two-dimensional electrophoresis reference map [J]. Electrophoresis, 21(16): 3483-3487.
[35]	Kannan K, Nelson AD, Shippen DE. 2008. Dyskerin is a component of the Arabidopsis telomerase RNP required for telomere maintenance [J]. Mol Cell Biol, 28(7): 2332-2341.
[36]	Kennedy BK, Austriaco NR Jr, Zhang J, Guarente L. 1995. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae [J]. Cell, 80(3): 485-496.
[37]	Kim SH, Koroleva OA, Lewandowska D, Pendle AF, Clark GP, Simpson CG, Shaw PJ, Brown JW. 2009. Aberrant mRNA transcripts and the nonsense-mediated decay proteins UPF2 and UPF3 are enriched in the Arabidopsis nucleolus [J]. Plant Cell, 21(7): 2045-2057.
[38]	Kim SH, Spensley M, Choi SK, Calixto CP, Pendle AF, Koroleva O, Shaw PJ, Brown JWS. 2010. Plant U13 orthologues and orphan snoRNAs identified by RNomics of RNA from Arabidopsis nucleoli [J]. Nucleic Acids Res, 38(9): 3054-3067.
[39]	Kobayashi T. 2008. A new role of the rDNA and nucleolus in the nucleus—rDNA instability maintains genome integrity [J]. BioEssays, 30(3): 267-272.
[40]	Koberna K, Malinsky J, Pliss A, Masata M, Vecerova J, Fialova M, Bednar J, Raska I. 2002. Ribosomal genes in focus: new transcripts label the dense fibrillar components and form clusters indicative of "Christmas trees" in situ [J]. J Cell Biol, 157(5): 743-748.
[41]	Kubota S, Siomi H, Satoh T, Endo S, Maki M, Hatanaka M. 1989. Functional similarity of HIV-I rev and HTLV-I rex proteins: identification of a new nucleolar-targeting signal in rev protein [J]. Biochem Biophys Res Commun, 162(3): 963-970.
[42]	Lamaye F, Galliot S, Alibardi L, Lafontaine DL, Thiry M. 2011. Nucleolar structure across evolution: the transition between bi- and tri-compartmentalized nucleoli lies within the class Reptilia [J]. J Struct Biol, 174(2): 352-359.
[43]	Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SW, Lagrange T, Pikaard CS, Jacobsen SE. 2006. An ARGONAUTE4- containing nuclear processing center colocalized with Cajal bodies in Arabidopsis Thaliana [J]. Cell, 126(1): 93-106.
[44]	Li JY. 1999. The primitive nucleus model and the origin of the cell nucleus [J]. Endocyt Cell Res, 13(1-3): 1-86.
[45]	Li JY, He YD, Chen SF. 1997. The primitive cell nucleus, in which the nucleolus has not emerged yet [J]. Endocyt Cell Res, 12(1-2): 65-70.
[46]	Liu JL, Murphy C, Buszczak M, Clatterbuck S, Goodman R, Gall JG. 2006. The Drosophila melanogaster Cajal body [J]. J Cell Biol, 172(6): 875-884.
[47]	Michienzi A, Cagnon L, Bahner I, Rossi JJ. 2000. Ribozyme-mediated inhibition of HIV 1 suggests nucleolar trafficking of HIV-1 RNA [J]. Proc Natl Acad Sci U S A, 97(16): 8955-8960.
[48]	Nathanson L, Xia T, Deutscher MP. 2003. Nuclear protein synthesis: a re-evaluation [J]. RNA, 9(1): 9-13.
[49]	Nie Y, Zhao Q, Su Y, Yang JH. 2004. Subcellular distribution of ADAR1 isoforms is synergistically determined by three nuclear discrimination signals and a regulatory motif [J]. J Biol Chem, 279(13): 13249-13255.
[50]	Olson MO, Hingorani K, Szebeni A. 2002. Conventional and nonconventional roles of the nucleolus [J]. Int Rev Cytol, 219: 199-266.
[51]	Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JW, Shaw PJ. 2005. Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions [J]. Mol Biol Cell, 16(1): 260-269.
[52]	Pliss A, Koberna K, Vecerova J, Malinsky J, Masata M, Fialova M, Raska I, Berezney R. 2005. Spatio-temporal dynamics at rDNA foci: global switching between DNA replication and transcription [J]. J Cell Biochem, 94(3): 554-565.
[53]	Politz JC, Lewandowski LB, Pederson T. 2002. Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis [J]. J Cell Biol, 159(3): 411-418.
[54]	Politz JC, Polena I, Trask I, Bazett-Jones DP, Pederson T. 2005. A nonribosomal landscape in the nucleolus revealed by the stem cell protein nucleostemin [J]. Mol Biol Cell, 16(7): 3401-3410.
[55]	Politz JC, Yarovoi S, Kilroy SM, Gowda K, Zwieb C, Pederson T. 2000. Signal recognition particle components in the nucleolus [J]. Proc Natl Acad Sci U S A, 97(1): 55-60.
[56]	Pontes O, Li CF, Costa Nunes P, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS. 2006. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center [J]. Cell, 126(1): 79-92.
[57]	Potashkin JA, Derby RJ, Spector DL. 1990. Differential distribution of factors involved in pre-mRNA processing in the yeast cell nucleus [J]. Mol Cell Biol, 10(7): 3524-3534.
[58]	Rubbi CP, Milner J. 2003. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses [J]. EMBO J, 22(22): 6068-6077.
[59]	Sallacz NB, Jantsch MF. 2005. Chromosomal storage of the RNA-editing enzyme ADAR1 in Xenopus oocytes [J]. Mol Biol Cell, 16(7): 3377-3386.
[60]	Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, Sanchez JC, Greco A, Hochstrasser D, Diaz JJ. 2002. Functional proteomic analysis of human nucleolus [J]. Mol Biol Cell, 13(11): 4100-4109.
[61]	Schneiter R, Kadowaki T, Tartakoff AM. 1995. mRNA transport in yeast: time to reinvestigate the functions of the nucleolus [J]. Mol Biol Cell, 6(4): 357-370.
[62]	Shaw PJ, Brown JW. 2012. Nucleoli: composition, function, and dynamics [J]. Plant Physiol, 158(1): 44-51.
[63]	Shaw PJ, Beven AF, Leader DJ, Brown JW. 1998. Localization and processing from a polycistronic precursor of novel snoRNAs in maize [J]. J Cell Sci, 111( Pt 15): 2121-2128.
[64]	Shaw PJ, Highett MI, Beven AF, Jordan EG. 1995. The nucleolar architecture of polymerase I transcription and processing [J]. EMBO J, 14(12): 2896-2906.
[65]	Siomi H, Shida H, Nam SH, Nosaka T, Maki M, Hatanaka M. 1988. Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing [J]. Cell, 55(2): 197-209.
[66]	Sommerville J, Brumwell CL, Politz JC, Pederson T. 2005. Signal recognition particle assembly in relation to the function of amplified nucleoli of Xenopus oocytes [J]. J Cell Sci, 118(Pt 6): 1299-1307.
[67]	Staub E, Mackowiak S, Vingron M. 2006. An inventory of yeast proteins associated with nucleolar and ribosomal components [J]. Genome Biol, 7(10): R98.
[68]	Staub E, Fiziev P, Rosenthal A, Hinzmann B. 2004. Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire [J]. Bioessays, 26(5): 567-581.
[69]	Steiner-Mosonyi M, Mangroo D. 2004. The nuclear tRNA aminoacylation- dependent pathway may be the principal route used to export tRNA from the nucleus in Saccharomyces cerevisiae [J]. Biochem J, 378(Pt 3): 809-816.
[70]	Tani T, Derby RJ, Hiraoka Y, Spector DL. 1995. Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport [J]. Mol Biol Cell, 6(11): 1515-1534.
[71]	Thiry M, Lafontaine DL. 2005. Birth of a nucleolus: the evolution of nucleolar compartments [J]. Trends Cell Biol, 15(4): 194-199.
[72]	Thiry M, Lamaye F, Lafontaine DL. 2011. The nucleolus: When 2 became 3 [J]. Nucleus, 2(4): 289-293.
[73]	Thompson M, Haeusler RA, Good PD, Engelke DR. 2003. Nucleolar clustering of dispersed tRNA genes [J]. Science, 302(5649): 1399-1401.
[74]	Visintin R, Amon A. 2000. The nucleolus: the magician's hat for cell cycle tricks [J]. Curr Opin Cell Biol, 12(6): 752.
[75]	Vitali P, Basyuk E, Le Meur E, Bertrand E, Muscatelli F, Cavaille J, Huttenhofer A. 2005. ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs [J]. J Cell Biol, 169(5): 745-753.
[76]	Wang L, Haeusler RA, Good PD, Thompson M, Nagar S, Engelke DR. 2005. Silencing near tRNA genes requires nucleolar localization [J]. J Biol Chem, 280(10): 8637-8639.
[77]	Warner JR. 1990. The nucleolus and ribosome formation [J]. Curr Opin Cell Biol, 2(3): 521-527.
[78]	Xin DD, Wen, JF. 2005. Ribosome biogenesis system of Giardia inferred from analysis of giardial genome [J]. Zool Res, 26(5): 484-491. [辛德东, 文建凡. 2005. 从基因组分析贾第虫的核糖体合成系统. 动物学研究, 26(5): 484-491.]
[79]	Xin DD, Wen, JF, He D, Lu SQ. 2005. Identification of a Giardia krr1 homolog gene and the secondarily anucleolate condition of Giardia lamblia [J]. Mol Biol Evol, 22(3): 391-394.
[80]	Yu YT, Shu MD, Narayanan A, Terns RM, Terns MP, Steitz JA. 2001. Internal modification of U2 small nuclear (sn)RNA occurs in nucleoli of Xenopus oocytes [J]. J Cell Biol, 152(6): 1279-1288.
[81]	Zhang S, Hemmerich P, Grosse F. 2004. Nucleolar localization of the human telomeric repeat binding factor 2 (TRF2) [J]. J Cell Sci, 117(Pt 17): 3935-3945.