Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells

Journal of Cell Biology

Volumn 166, Issue 6, 2004, Pages 787-800

  Leung, Anthony Kar Lun ^a,c   Gerlich, Daniel ^b   Miller, Gail ^a,d   Lyon, Carol ^a,e   Lam, Yun Wah ^a   Lleres, David ^a   Daigle, Nathalie ^b   Zomerdijk, Joost ^a   Ellenberg, Jan ^b   Lamond, Angus I ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e CYCLACEL LTD   (United Kingdom)

Author keywords

4D imaging; Fluorescent protein; Mitosis; Nucleolus; Nucleus

Indexed keywords

FLUORESCENT DYE; RNA POLYMERASE;

ARTICLE; CELL DIVISION; CELL NUCLEUS; CONTROLLED STUDY; HUMAN; HUMAN CELL; KINETICS; MITOSIS; MOLECULAR DYNAMICS; NUCLEOLUS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS;

CELL NUCLEOLUS; FLUORESCENT DYES; HELA CELLS; HUMANS; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; KINETICS; MITOSIS; MODELS, BIOLOGICAL; NUCLEAR ENVELOPE; NUCLEOLUS ORGANIZER REGION; PRECIPITIN TESTS; RNA POLYMERASE I;

MAMMALIA;

EID: 4544330157     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200405013     Document Type: Article

References (40)

1. Beaudouin, J., D. Gerlich, N. Daigle, R. Eils, and J. Ellenberg. 2002. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell. 108:83-96.
2. Bickmore, W.A., and J.R. Chubb. 2003. Dispatch. Chromosome position: now, where was I? Curr. Biol. 13:R357-R359.
3. Burke, B., and J. Ellenberg. 2002. Remodelling the walls of the nucleus. Nat. Rev. Mol. Cell Biol. 3:487-497.
4. Carmo-Fonseca, M., L. Mendes-Soares, and I. Campos. 2000. To be or not to be in the nucleolus. Nat. Cell Biol. 2:E107-E112.
5. Clute, P., and J. Pines. 1999. Temporal and spatial control ofcyclin BI destruction in metaphase. Nat. Cell Biol. 1:82-87.
6. Conconi, A., R.M. Widmer, T. Koller, and J.M. Sogo. 1989. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell. 57:753-761.
7. Dundr, M., T. Misteli, and M.O. Olson. 2000. The dynamics of postmitotic reassembly of the nucleolus. J. Cell Biol. 150:433-446.
8. Dundr, M., U. Hoffmann-Rohrer, Q. Hu, I. Grummt, L.I. Rothblum, R.D. Phair, and T. Misteli. 2002a. A kinetic framework for a mammalian RNA polymerase in vivo. Science. 298:1623-1626.
9. Dundr, M., J.G. McNally, J. Cohen, and T. Misteli. 2002b. Quantitation of GFP-fusion proteins in single living cells. J. Struct. Biol. 140:92-99.
10. Gerbi, S.A., A.V. Borovjagin, and T.S. Lange. 2003. The nucleolus: a site of ribonucleoprotein maturation. Curr. Opin. Cell Biol. 15:318-325.
11. Gerlich, D., and J. Ellenberg. 2003a. 4D imaging to assay complex dynamics in live specimens. Nat. Cell Biol. 5:S14-S19.
12. Gerlich, D., and J. Ellenberg. 2003b. Dynamics of chromosome positioning during the cell cycle. Curr. Opin. Cell Biol. 15:664-671.
13. Gerlich, D., J. Beaudouin, M. Gebhard, J. Ellenberg, and R. Eils. 2001. Four-dimensional imaging and quantitative reconstruction to analyse complex spatiotemporal processes in live cells. Nat. Cell Biol. 3:852-855.
14. Gilbert, N., L. Lucas, C. Klein, M. Menager, N. Bonnet, and D. Ploton. 1995. Three-dimensional co-location of RNA polymerase 1 and DNA during interphase and mitosis by confocal microscopy. J. Cell Sci. 108:115-125.
15. Gonda, K., J. Fowler, N. Katoku-Kikyo, J. Haroldson, J. Wudel, and N. Kikyo. 2003. Reversible disassembly of somatic nucleoli by the germ cell proteins FRGY2a and FRGY2b. Nat. Cell Biol. 5:205-210.
16. Heix, J., A. Vente, R. Voit, A. Budde, T.M. Michaelidis, and I. Grummt. 1998. Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phosphorylation. EMBO J. 17:7373-7381.
17. Hernandez-Verdun, D., P. Roussel, and J. Gebrane-Younes. 2002. Emerging concepts of nucleolar assembly. J. Cell Sci. 115:2265-2270.
18. Huang, S. 2002. Building an efficient factory: where is pre-rRNA synthesized in the nucleolus? J. Cell Biol. 157:739-741.
19. Janicki, S.M., and D.L. Spector. 2003. Nuclear choreography: interpretations from living cells. Curr. Opin. Cell Biol. 15:149-157.
20. Jimenez-Garcia, L.F., M.L. Segura-Valdez, R.L. Ochs, L.I. Rothblum, R. Hannan, and D.L. Spector. 1994. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol. Biol. Cell. 5:955-966.
21. Jones, E., H. Kimura, M. Vigneron, Z. Wang, R.G. Roeder, and P.R. Cook. 2000. Isolation and characterization of monoclonal antibodies directed against subunits of human RNA polymerases 1, 11 and 111. Exp. Cell Res. 254:163-172.
22. Jordan, P., M. Mannervik, L. Tora, and M. Carmo-Fonseca. 1996. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase 1 when rRNA synthesis is either active or inactive. J. Cell Biol. 133:225-234.
23. Klein, J., and I. Grummt. 1999. Cell cycle-dependent regulation of RNA polymerase I transcription: the nucleolar transcription factor UBF is inactive in mitosis and early G1. Proc. Natl. Acad. Sci. USA. 96:6096-6101.
24. Leung, A.K., and A.I. Lamond. 2002. In vivo analysis of NHPX reveals a novel nucleolar localization pathway involving a transient accumulation in splicing speckles. J. Cell Biol. 157:615-629.
25. Leung, A.K., and A.I. Lamond. 2003. The dynamics of the nucleolus. Crit. Rev. Eukaryot. Gene Expr. 13:39-54.
26. Levsky, J.M., S.M. Shenoy, R.C. Pezo, and R.H. Singer. 2002. Single-cell gene expression profiling. Science. 297:836-840.
27. Miller, G., K.I. Panov, J.K. Friedrich, L. Trinkle-Mulcahy, A.I. Lamond, and J.C. Zomerdijk. 2001. hRRN3 is essential in the SL1-mediated recruitment of RNA Polymerase I to rRNA gene promoters. EMBO J. 20:1373-1382.
28. Oison, M.O., M. Dundr, and A. Szebeni. 2000. The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol. 10:189-196.
29. Parada, L., and T. Misteli. 2002. Chromosome posirioning in the interphase nucleus. Trends Cell Biol. 12:425-432.
30. Pines, J., and C.L. Rieder. 2001. Re-staging mitosis: a contemporary view of mitotic progression. Nat. Cell Biol. 3:E3-E6.
31. Prasanth, K.V., P.A. Sacco-Bubulya, S.G. Prasanth, and D.L. Spector. 2003. Sequential entry of components of the gene expression machinery into daughter nuclei. Mol. Biol. Cell. 14:1043-1057.
32. Roussel, P., C. Andre, C. Masson, G. Geraud, and D. Hernandez-Verdun. 1993. Localization of the RNA polymerase I transcription factor hUBF during the cell cycle. J. Cell Sci. 104:327-337.
33. Rubbi, C.P., and J. Milner. 2003. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 22:6068-6077.
34. Savino, T.M., J. Gebrane-Younes, J. De Mey, J.B. Sibarita, and D. Hernandez-Verdun. 2001. Nucleolar assembly of the rRNA processing machinery in living cells. J. Cell Biol. 153:1097-1110.
35. Scheer, U., and K.M. Rose. 1984. Localization of RNA polymerase 1 in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. Proc. Natl. Acad. Sci. USA. 81:1431-1435.
36. Sirri, V., P. Roussel, and D. Hernandez-Verdun. 2000. In vivo release of mitotic silencing of ribosomal gene transcription does not give rise to precursor ribosomal RNA processing. J. Cell Biol. 148:259-270.
37. Sirri, V., D. Hernandez-Verdun, and P. Roussel. 2002. Cyclin-dependent kinases govern formation and maintenance of the nucleolus. J. Cell Biol. 156:969-981.
38. Thomson, I., S. Gilchrist, W.A. Bickmore, and J.R. Chubb. 2004. The radial positioning of chromatin is not inherited through mitosis but is established de novo in early G1. Curr. Biol. 14:166-172.
39. Walter, J., L. Schermelleh, M. Cremer, S. Tashiro, and T. Cremer. 2003. Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J. Cell Biol. 160:685-697.
40. Weisenberger, D., and U. Scheer. 1995. A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J. Cell Biol. 129:561-575.