Centromeres direct chromosomal inheritance by nucleating assembly of the kinetochore, a large multiprotein complex required for microtubule attachment during mitosis. Centromere identity in humans is epigenetically determined, with no DNA sequence either necessary or sufficient. A prime candidate for the epigenetic mark is assembly into centromeric chromatin of centromere protein A (CENP-A), a histone H3 variant found only at functional centromeres. A new covalent fluorescent pulse-chase labeling approach using SNAP tagging has now been developed and is used to demonstrate that CENP-A bound to a mature centromere is quantitatively and equally partitioned to sister centromeres generated during S phase, thereby remaining stably associated through multiple cell divisions. Loading of nascent CENP-A on the megabase domains of replicated centromere DNA is shown to require passage through mitosis but not microtubule attachment. Very surprisingly, assembly and stabilization of new CENP-A–containing nucleosomes is restricted exclusively to the subsequent G1 phase, demonstrating direct coupling between progression through mitosis and assembly/maturation of the next generation of centromeres.
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12 March 2007
Article|
March 05 2007
Propagation of centromeric chromatin requires exit from mitosis
In Special Collection:
JCB65: Cell Division, Cell Cycle, and Polarity
Lars E.T. Jansen,
Lars E.T. Jansen
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
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Ben E. Black,
Ben E. Black
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
2Department of Biochemistry and Biophysics, University of Pennsylvania School of Medicine, Philadelphia, PA 19104
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Daniel R. Foltz,
Daniel R. Foltz
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
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Don W. Cleveland
Don W. Cleveland
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
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Lars E.T. Jansen
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
Ben E. Black
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
2Department of Biochemistry and Biophysics, University of Pennsylvania School of Medicine, Philadelphia, PA 19104
Daniel R. Foltz
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
Don W. Cleveland
1Ludwig Institute for Cancer Research and Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093
Correspondence to Don W. Cleveland: [email protected]
Abbreviations used in this paper: BG, benzylguanine; CENP-A, centromere protein A; PEG, polyethylene glycol; TMR, tetramethylrhodamine.
Received:
January 11 2007
Accepted:
February 07 2007
Online ISSN: 1540-8140
Print ISSN: 0021-9525
The Rockefeller University Press
2007
J Cell Biol (2007) 176 (6): 795–805.
Article history
Received:
January 11 2007
Accepted:
February 07 2007
Citation
Lars E.T. Jansen, Ben E. Black, Daniel R. Foltz, Don W. Cleveland; Propagation of centromeric chromatin requires exit from mitosis . J Cell Biol 12 March 2007; 176 (6): 795–805. doi: https://doi.org/10.1083/jcb.200701066
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