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Published online 7 September 2004. doi:10.1083/jcb.200405013
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 166, Number 6, 787-800
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Article

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

Anthony Kar Lun Leung1, Daniel Gerlich2, Gail Miller1, Carol Lyon1, Yun Wah Lam1, David Lleres1, Nathalie Daigle2, Joost Zomerdijk1, Jan Ellenberg2, and Angus I. Lamond1

1 Division of Gene Regulation and Expression, School of Life Sciences, Wellcome Trust Biocentre, University of Dundee, Dundee DD1 5EH, Scotland, UK
2 European Molecular Biology Laboratory (EMBL), D6901 Heidelberg, Germany

Address correspondence to Angus I. Lamond, Division of Gene Regulation and Expression, School of Life Sciences, Wellcome Trust Biocentre, University of Dundee. Dundee DD1 5EH, Scotland, UK. Tel.: 44-1382-345473. Fax: 44-1382-345695. email: a.i.lamond{at}dundee.ac.uk

One of the great mysteries of the nucleolus surrounds its disappearance during mitosis and subsequent reassembly at late mitosis. Here, the relative dynamics of nucleolar disassembly and reformation were dissected using quantitative 4D microscopy with fluorescent protein-tagged proteins in human stable cell lines. The data provide a novel insight into the fates of the three distinct nucleolar subcompartments and their associated protein machineries in a single dividing cell. Before the onset of nuclear envelope (NE) breakdown, nucleolar disassembly started with the loss of RNA polymerase I subunits from the fibrillar centers. Dissociation of proteins from the other subcompartments occurred with faster kinetics but commenced later, coincident with the process of NE breakdown. The reformation pathway also follows a reproducible and defined temporal sequence but the order of reassembly is shown not to be dictated by the order in which individual nucleolar components reaccumulate within the nucleus after mitosis.

Key Words: nucleolus; nucleus; mitosis; fluorescent protein; 4D imaging

A.K.L. Leung's present address is Center for Cancer Research, Dept. of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139.

G. Miller's present address is Fred Hutchinson Cancer Research Center, MS A1-162, 1100 Fairview Ave. N., Seattle, WA 9810.

C. Lyon's present address is Cyclacel, James Lindsay Place, Dundee Technopole, Dundee DD1 5JJ, UK.

Abbreviations used in this paper: B23, nucleophosmin/nucleolar phosphoprotein B23/numatrin; DFC, dense fibrillar component; FC, fibrillar centre; FIB, fibrillarin; FP, fluorescent protein; GC, granular component; IBB, importin-ß binding; LB1, lamin B1; LBR, lamin B receptor; NE, nuclear envelope; NOR, nucleolar organizing region; PNB, prenucleolar body; rDNA, ribosomal DNA; RL27, ribosomal protein L27; RPA39, RNA polymerase I subunit RPA39; RRN3, RNA polymerase I transcription factor RRN3; UBF, upstream binding transcription factor.


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