The Nucleolus under Stress

Molecular Cell

Volumn 40, Issue 2, 2010, Pages 216-227

  Boulon, Séverine ^a   Westman, Belinda J ^a   Hutten, Saskia ^a   Boisvert, François Michel ^a   Lamond, Angus I ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; PROTEIN P53; RIBOSOME PROTEIN;

CELL STRESS; COILED BODY; HUMAN; MOLECULAR INTERACTION; NONHUMAN; NUCLEOLUS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; RIBOSOME SUBUNIT; SIGNAL TRANSDUCTION;

ANIMALS; CELL NUCLEOLUS; CELL NUCLEUS; COILED BODIES; DNA REPAIR; HUMANS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

MAMMALIA;

EID: 78649336111     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.09.024     Document Type: Review

References (112)

1. Ahmad Y., Boisvert F.M., Gregor P., Cobley A., Lamond A.I. NOPdb: Nucleolar Proteome Database-2008 update. Nucleic Acids Res. 2009, 37:D181-D184.
2. Al-Baker E.A., Oshin M., Hutchison C.J., Kill I.R. Analysis of UV-induced damage and repair in young and senescent human dermal fibroblasts using the comet assay. Mech. Ageing Dev. 2005, 126:664-672.
3. Andersen J.S., Lam Y.W., Leung A.K., Ong S.E., Lyon C.E., Lamond A.I., Mann M. Nucleolar proteome dynamics. Nature 2005, 433:77-83.
4. Andrade L.E., Tan E.M., Chan E.K. Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation. Proc. Natl. Acad. Sci. USA 1993, 90:1947-1951.
5. Banerjee R., Weidman M.K., Navarro S., Comai L., Dasgupta A. Modifications of both selectivity factor and upstream binding factor contribute to poliovirus-mediated inhibition of RNA polymerase I transcription. J. Gen. Virol. 2005, 86:2315-2322.
6. Banski P., Kodiha M., Stochaj U. Chaperones and multitasking proteins in the nucleolus: networking together for survival?. Trends Biochem. Sci. 2010, 35:361-367.
7. Banski P., Mahboubi H., Kodiha M., Shrivastava S., Kanagaratham C., Stochaj U. Nucleolar targeting of the chaperone HSC70 is regulated by stress, cell signaling and a composite targeting signal which is controlled by autoinhibition. J. Biol. Chem. 2010, 285:21858-21867.
8. Bassermann F., Frescas D., Guardavaccaro D., Busino L., Peschiaroli A., Pagano M. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 2008, 134:256-267.
9. Belin S., Kindbeiter K., Hacot S., Albaret M.A., Roca-Martinez J.X., Therizols G., Grosso O., Diaz J.J. Uncoupling ribosome biogenesis regulation from RNA polymerase I activity during herpes simplex virus type 1 infection. RNA 2010, 16:131-140.
10. Berciano M.T., Novell M., Villagra N.T., Casafont I., Bengoechea R., Val-Bernal J.F., Lafarga M. Cajal body number and nucleolar size correlate with the cell body mass in human sensory ganglia neurons. J. Struct. Biol. 2007, 158:410-420.
11. Boisvert F.M., Lamond A.I. P53-dependent subcellular proteome localization following DNA damage. Proteomics. 2010, 10.1002/pmic.201000213.
12. Boisvert F.M., van Koningsbruggen S., Navascues J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8:574-585.
13. Boisvert F.M., Lam Y.W., Lamont D., Lamond A.I. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 2010, 9:457-470.
14. Bongiorno-Borbone L., De Cola A., Barcaroli D., Knight R.A., Di Ilio C., Melino G., De Laurenzi V. FLASH degradation in response to UV-C results in histone locus bodies disruption and cell-cycle arrest. Oncogene 2010, 29:802-810.
15. Burger K., Muhl B., Harasim T., Rohrmoser M., Malamoussi A., Orban M., Kellner M., Gruber-Eber A., Kremmer E., Holzel M., Eick D. Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J. Biol. Chem. 2010, 285:12416-12425.
16. Caldarola S., De Stefano M.C., Amaldi F., Loreni F. Synthesis and function of ribosomal proteins-fading models and new perspectives. FEBS J. 2009, 276:3199-3210.
17. Carmo-Fonseca M., Pepperkok R., Carvalho M.T., Lamond A.I. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J. Cell Biol. 1992, 117:1-14.
18. Carmo-Fonseca M., Ferreira J., Lamond A.I. Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis-evidence that the coiled body is a kinetic nuclear structure. J. Cell Biol. 1993, 120:841-852.
19. Carter S., Vousden K.H. Modifications of p53: competing for the lysines. Curr. Opin. Genet. Dev. 2009, 19:18-24.
20. Chedin S., Laferte A., Hoang T., Lafontaine D.L., Riva M., Carles C. Is ribosome synthesis controlled by pol I transcription?. Cell Cycle 2007, 6:11-15.
21. Chen D., Shan J., Zhu W.G., Qin J., Gu W. Transcription-independent ARF regulation in oncogenic stress-mediated p53 responses. Nature 2010, 464:624-627.
22. Cioce M., Lamond A.I. Cajal bodies: a long history of discovery. Annu. Rev. Cell Dev. Biol. 2005, 21:105-131.
23. Cioce M., Boulon S., Matera A.G., Lamond A.I. UV-induced fragmentation of Cajal bodies. J. Cell Biol. 2006, 175:401-413.
24. Cohen A.A., Geva-Zatorsky N., Eden E., Frenkel-Morgenstern M., Issaeva I., Sigal A., Milo R., Cohen-Saidon C., Liron Y., Kam Z., et al. Dynamic proteomics of individual cancer cells in response to a drug. Science 2008, 322:1511-1516.
25. David-Pfeuty T. Potent inhibitors of cyclin-dependent kinase 2 induce nuclear accumulation of wild-type p53 and nucleolar fragmentation in human untransformed and tumor-derived cells. Oncogene 1999, 18:7409-7422.
26. Deisenroth C., Zhang Y. Ribosome biogenesis surveillance: probing the ribosomal protein-Mdm2-p53 pathway. Oncogene 2010, 29:4253-4260.
27. Emmott E., Hiscox J.A. Nucleolar targeting: the hub of the matter. EMBO Rep. 2009, 10:231-238.
28. Emmott E., Rodgers M., Macdonald A., McCrory S., Ajuh P., Hiscox J.A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture (SILAC) reveals changes in the cytoplasmic, nuclear and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol. Cell. Proteomics 2010, 9:5335-5345.
29. Fontoura B.M., Sorokina E.A., David E., Carroll R.B. p53 is covalently linked to 5.8S rRNA. Mol. Cell. Biol. 1992, 12:5145-5151.
30. Fumagalli S., Di Cara A., Neb-Gulati A., Natt F., Schwemberger S., Hall J., Babcock G.F., Bernardi R., Pandolfi P.P., Thomas G. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat. Cell Biol. 2009, 11:501-508.
31. Gall J.G. Cajal bodies: the first 100 years. Annu. Rev. Cell Dev. Biol. 2000, 16:273-300.
32. Gil J., Peters G. Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat. Rev. Mol. Cell Biol. 2006, 7:667-677.
33. Gjerset R.A., Bandyopadhyay K. Regulation of p14ARF through subnuclear compartmentalization. Cell Cycle 2006, 5:686-690.
34. Govoni M., Farabegoli F., Pession A., Novello F. Inhibition of topoisomerase II activity and its effect on nucleolar structure and function. Exp. Cell Res. 1994, 211:36-41.
35. Greco A. Involvement of the nucleolus in replication of human viruses. Rev. Med. Virol. 2009, 19:201-214.
36. Greco A., Di Benedetto A., Howard C.M., Kelly S., Nande R., Dementieva Y., Miranda M., Brunetti A., Salvatore M., Claudio L., et al. Eradication of therapy-resistant human prostate tumors using an ultrasound-guided site-specific cancer terminator virus delivery approach. Mol. Ther. 2010, 18:295-306.
37. Gridasova A.A., Henry R.W. The p53 tumor suppressor protein represses human snRNA gene transcription by RNA polymerases II and III independently of sequence-specific DNA binding. Mol. Cell. Biol. 2005, 25:3247-3260.
38. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 2003, 17:1691-1702.
39. Grummt I., Voit R. Linking rDNA transcription to the cellular energy supply. Cell Cycle 2010, 9:225-226.
40. Haaf T., Ward D.C. Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp. Cell Res. 1996, 224:163-173.
41. Handwerger K.E., Wu Z., Murphy C., Gall J.G. Heat shock induces mini-Cajal bodies in the Xenopus germinal vesicle. J. Cell Sci. 2002, 115:2011-2020.
42. Hardie D.G. New roles for the LKB1→AMPK pathway. Curr. Opin. Cell Biol. 2005, 17:167-173.
43. Hebert M.D. Phosphorylation and the Cajal body: modification in search of function. Arch. Biochem. Biophys. 2010, 496:69-76.
44. Henras A.K., Soudet J., Gerus M., Lebaron S., Caizergues-Ferrer M., Mougin A., Henry Y. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 2008, 65:2334-2359.
45. Hiscox J.A. RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol. 2007, 5:119-127.
46. Hock A., Vousden K.H. Regulation of the p53 pathway by ubiquitin and related proteins. Int. J. Biochem. Cell Biol. 2010, 42:1618-1621.
47. Holzel M., Orban M., Hochstatter J., Rohrmoser M., Harasim T., Malamoussi A., Kremmer E., Langst G., Eick D. Defects in 18 S or 28 S rRNA processing activate the p53 pathway. J. Biol. Chem. 2010, 285:6364-6370.
48. Hoppe S., Bierhoff H., Cado I., Weber A., Tiebe M., Grummt I., Voit R. AMP-activated protein kinase adapts rRNA synthesis to cellular energy supply. Proc. Natl. Acad. Sci. USA 2009, 106:17781-17786.
49. James M.J., Zomerdijk J.C. Phosphatidylinositol 3-kinase and mTOR signaling pathways regulate RNA polymerase I transcription in response to IGF-1 and nutrients. J. Biol. Chem. 2004, 279:8911-8918.
50. James N.J., Howell G.J., Walker J.H., Blair G.E. The role of Cajal bodies in the expression of late phase adenovirus proteins. Virology 2010, 399:299-311.
51. Kaiser T.E., Intine R.V., Dundr M. De novo formation of a subnuclear body. Science 2008, 322:1713-1717.
52. Kao C.F., Chen S.Y., Lee Y.H. Activation of RNA polymerase I transcription by hepatitis C virus core protein. J. Biomed. Sci. 2004, 11:72-94.
53. Kim S.H., Ryabov E.V., Kalinina N.O., Rakitina D.V., Gillespie T., MacFarlane S., Haupt S., Brown J.W., Taliansky M. Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO J. 2007, 26:2169-2179.
54. Kiss T., Fayet E., Jady B.E., Richard P., Weber M. Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb. Symp. Quant. Biol. 2006, 71:407-417.
55. Kressler D., Hurt E., Bassler J. Driving ribosome assembly. Biochim. Biophys. Acta 2010, 1803:673-683.
56. Kruhlak M., Crouch E.E., Orlov M., Montano C., Gorski S.A., Nussenzweig A., Misteli T., Phair R.D., Casellas R. The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature 2007, 447:730-734.
57. Kruse J.P., Gu W. SnapShot: p53 posttranslational modifications. Cell 2008, 133:930-930.e1.
58. Kruse J.P., Gu W. Modes of p53 regulation. Cell 2009, 137:609-622.
59. Lafarga M., Casafont I., Bengoechea R., Tapia O., Berciano M.T. Cajal's contribution to the knowledge of the neuronal cell nucleus. Chromosoma 2009, 118:437-443.
60. Lam Y.W., Evans V.C., Heesom K.J., Lamond A.I., Matthews D.A. Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol. Cell. Proteomics 2010, 9:117-130.
61. Lee J.T., Gu W. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ. 2010, 17:86-92.
62. Lemm I., Girard C., Kuhn A.N., Watkins N.J., Schneider M., Bordonne R., Luhrmann R. Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. Mol. Biol. Cell 2006, 17:3221-3231.
63. Lempiainen H., Shore D. Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 2009, 21:855-863.
64. Li Z., Hann S.R. The Myc-nucleophosmin-ARF network: a complex web unveiled. Cell Cycle 2009, 8:2703-2707.
65. Lindstrom M.S. Emerging functions of ribosomal proteins in gene-specific transcription and translation. Biochem. Biophys. Res. Commun. 2009, 379:167-170.
66. Lyon C.E., Bohmann K., Sleeman J., Lamond A.I. Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus. Exp. Cell Res. 1997, 230:84-93.
67. Mao I., Liu J., Li X., Luo H. REGgamma, a proteasome activator and beyond?. Cell. Mol. Life Sci. 2008, 65:3971-3980.
68. Marzluff W.F., Wagner E.J., Duronio R.J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 2008, 9:843-854.
69. Matera A.G. Drosophila Cajal bodies: accessories not included. J. Cell Biol. 2006, 172:791-793.
70. Matera A.G., Terns R.M., Terns M.P. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat. Rev. Mol. Cell Biol. 2007, 8:209-220.
71. Mayer C., Grummt I. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 2006, 25:6384-6391.
72. McGowan K.A., Li J.Z., Park C.Y., Beaudry V., Tabor H.K., Sabnis A.J., Zhang W., Fuchs H., de Angelis M.H., Myers R.M., et al. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat. Genet. 2008, 40:963-970.
73. McStay B., Grummt I. The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol. 2008, 24:131-157.
74. Mekhail K., Rivero-Lopez L., Khacho M., Lee S. Restriction of rRNA synthesis by VHL maintains energy equilibrium under hypoxia. Cell Cycle 2006, 5:2401-2413.
75. Montanaro L., Trere D., Derenzini M. Nucleolus, ribosomes, and cancer. Am. J. Pathol. 2008, 173:301-310.
76. Morency E., Sabra M., Catez F., Texier P., Lomonte P. A novel cell response triggered by interphase centromere structural instability. J. Cell Biol. 2007, 177:757-768.
77. Moss T., Langlois F., Gagnon-Kugler T., Stefanovsky V. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 2007, 64:29-49.
78. Murayama A., Ohmori K., Fujimura A., Minami H., Yasuzawa-Tanaka K., Kuroda T., Oie S., Daitoku H., Okuwaki M., Nagata K., et al. Epigenetic control of rDNA loci in response to intracellular energy status. Cell 2008, 133:627-639.
79. Narla A., Ebert B.L. Ribosomopathies: human disorders of ribosome dysfunction. Blood 2010, 115:3196-3205.
80. Navascues J., Bengoechea R., Tapia O., Casafont I., Berciano M.T., Lafarga M. SUMO-1 transiently localizes to Cajal bodies in mammalian neurons. J. Struct. Biol. 2008, 163:137-146.
81. Nizami Z., Deryusheva S., Gall J.G. The Cajal body and histone locus body. Cold Spring Harb. Perspect. Biol. 2010, 2. Published online May 26, 2010. 10.1101/cshperspect.a000653.
82. Ofir-Rosenfeld Y., Boggs K., Michael D., Kastan M.B., Oren M. Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol. Cell 2008, 32:180-189.
83. Olson M.O. Sensing cellular stress: another new function for the nucleolus?. Sci. STKE 2004, 2004:pe10.
84. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
85. Pederson T., Tsai R.Y. In search of nonribosomal nucleolar protein function and regulation. J. Cell Biol. 2009, 184:771-776.
86. Rebelo L., Almeida F., Ramos C., Bohmann K., Lamond A.I., Carmo-Fonseca M. The dynamics of coiled bodies in the nucleus of adenovirus-infected cells. Mol. Biol. Cell 1996, 7:1137-1151.
87. Riley K.J., Maher L.J. p53 RNA interactions: new clues in an old mystery. RNA 2007, 13:1825-1833.
88. Rubbi C.P., Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 2003, 22:6068-6077.
89. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
90. Sengupta S., Peterson T.R., Sabatini D.M. Regulation of the mTor complex 1 by nutrients, growth factors, and stress. Mol. Cell 2010, 40:310-322. this issue.
91. Shav-Tal Y., Blechman J., Darzacq X., Montagna C., Dye B.T., Patton J.G., Singer R.H., Zipori D. Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol. Biol. Cell 2005, 16:2395-2413.
92. Sherr C.J. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 2006, 6:663-673.
93. Sirri V., Urcuqui-Inchima S., Roussel P., Hernandez-Verdun D. Nucleolus: the fascinating nuclear body. Histochem. Cell Biol. 2008, 129:13-31.
94. Sleeman J.E., Ajuh P., Lamond A.I. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J. Cell Sci. 2001, 114:4407-4419.
95. Stanek D., Neugebauer K.M. The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze. Chromosoma 2006, 115:343-354.
96. Stehmeier P., Muller S. Regulation of p53 family members by the ubiquitin-like SUMO system. DNA Repair (Amst.) 2009, 8:491-498.
97. Strzelecka M., Trowitzsch S., Weber G., Luhrmann R., Oates A.C., Neugebauer K.M. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat. Struct. Mol. Biol. 2010, 17:403-409.
98. Sundqvist A., Liu G., Mirsaliotis A., Xirodimas D.P. Regulation of nucleolar signalling to p53 through NEDDylation of L11. EMBO Rep. 2009, 10:1132-1139.
99. Tanaka Y., Okamoto K., Teye K., Umata T., Yamagiwa N., Suto Y., Zhang Y., Tsuneoka M. JmjC enzyme KDM2A is a regulator of rRNA transcription in response to starvation. EMBO J. 2010, 29:1510-1522.
100. Tapia O., Bengoechea R., Berciano M.T., Lafarga M. Nucleolar targeting of coilin is regulated by its hypomethylation state. Chromosoma 2010, 119:527-540.
101. Thoms H.C., Loveridge C.J., Simpson J., Clipson A., Reinhardt K., Dunlop M.G., Stark L.A. Nucleolar targeting of RelA(p65) is regulated by COMMD1-dependent ubiquitination. Cancer Res. 2010, 70:139-149.
102. Tschochner H., Hurt E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 2003, 13:255-263.
103. Verheggen C., Lafontaine D.L., Samarsky D., Mouaikel J., Blanchard J.M., Bordonne R., Bertrand E. Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. EMBO J. 2002, 21:2736-2745.
104. Vousden K.H., Prives C. Blinded by the light: the growing complexity of p53. Cell 2009, 137:413-431.
105. Walker M.P., Tian L., Matera A.G. Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS ONE 2009, 4:e6171. 10.1371/journal.pone.0006171.
106. Warner J.R., McIntosh K.B. How common are extraribosomal functions of ribosomal proteins?. Mol. Cell 2009, 34:3-11.
107. Xiao L., Grove A. Coordination of ribosomal protein and ribosomal RNA gene expression in response to TOR signaling. Curr. Genomics 2009, 10:198-205.
108. Young P.J., Day P.M., Zhou J., Androphy E.J., Morris G.E., Lorson C.L. A direct interaction between the survival motor neuron protein and p53 and its relationship to spinal muscular atrophy. J. Biol. Chem. 2002, 277:2852-2859.
109. Zhai W., Comai L. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol. Cell. Biol. 2000, 20:5930-5938.
110. Zhang Y., Xiong Y. Mutations in human ARF exon 2 disrupt its nucleolar localization and impair its ability to block nuclear export of MDM2 and p53. Mol. Cell 1999, 3:579-591.
111. Zhang Y., Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell 2009, 16:369-377.
112. Zhou Y., Schmitz K.M., Mayer C., Yuan X., Akhtar A., Grummt I. Reversible acetylation of the chromatin remodelling complex NoRC is required for non-coding RNA-dependent silencing. Nat. Cell Biol. 2009, 11:1010-1016.