Propagation of centromeric chromatin requires exit from mitosis

By L. Jansen, B. E. Black, D. Foltz, D. Cleveland. Journal of Cell Biology, 2007

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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.

Subfields: Cell Biology, Molecular Biology, Plant Science

View Paper: https://www.semanticscholar.org/paper/4462a519e572714d1e88ca1db2536c804a557721

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Citations in the corpus

Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division (2014, background): “…manner (Mello and Almouzni, 2001), newly synthesized CENP-A is deposited during the subsequent mitosis, in telophase and G1 in human cells (Jansen et al., 2007), during metaphase in D. melanogaster S2 cells (Mellone et al., 2011), and anaphase in the syncytial D. melanogaster embryos…”
From telomere to telomere: the transcriptional and epigenetic state of human repeat elements (2021, background): “Since centromere transcription and CENP-A deposition are dynamic processes (89), we set out to test whether satellite transcription varied across the cell cycle.”
Epigenetic inheritance during the cell cycle (2009, background): “Recent evidence in mammalian cells now suggests that the loading of new CENP-A onto centromeres is restricted to a discrete cell cycle window in late telophase–early G1 phas”
An engineered protein tag for multiprotein labeling in living cells. (2008, methodology): “Prominent examples of such pulse-chase experiments include the study of gap junction plaque formation through pulsechase labeling of connexin-43 using the tetracysteine tag (Gaietta et al., 2002) and the determination of the time point of insertion of CENP-A in centromeres during the cell cycle usin”
Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. (2009, positive): “…complex is recruited to centromeres beginning in late anaphase and persists for approximately 3 hr 476 Cell 137, 472–484, May 1, 2009 ª2009 Elsevier Inc. after metaphase, which overlaps with the time during which new CENP-A is recruited to centromeres (Fujita et al., 2007; Jansen et al., 2007).”
HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. (2009, positive): “HJURP Associates with Centromeres during Late Telophase/Early G1 Phase As HJURP localization onto chromatin appeared to coincide precisely with the short time window when new CENP-A is loaded at centromeres (Jansen et al., 2007), we assessed whether HJURP associates with centromeres at this time.”