Distinct modes of centromere protein dynamics during cell cycle progression in <i>Drosophila</i> S2R+ cells

Lidsky, Peter V.; Sprenger, Frank; Lehner, Christian F.

doi:10.1242/jcs.134122

Cited by 31 publications

(53 citation statements)

References 83 publications

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“…Although plasmid supercoiling assay previously demonstrated that the subregion (1-160) of CAL1 lacking the self-association domain is sufficient for dCENP-A nucleosome assembly activity in vitro , excess of dCENP-A/H4/CAL1 complex under these conditions might be sufficient to overcome the self-association requirement observed in vivo. A role for dCENP-C as a stable platform for CAL1/dCENP-A recruitment is further supported by experiments indicating that dCENP-C is stably bound to centromeres (Lidsky et al, 2013;Mellone et al, 2011).…”

Section: Discussionmentioning

confidence: 78%

“…To ensure epigenetic inheritance the centromere mark must stably persist through the multiple division cycles of a cell. Unlike canonical histone H3, CENP-A nucleosomes are not replenished during DNA replication but from late mitosis through G1 phase (Dunleavy et al, 2012;Jansen et al, 2007;Lidsky et al, 2013;Schuh et al, 2007). One attractive model for the self-propagation of CENP-A is an epigenetic loop, where one or more adaptors recognize and direct the deposition of new CENP-A.…”

Section: Introductionmentioning

confidence: 99%

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Epigenetic inheritance of centromere identity in a heterologous system

Roure

Medina‐Pritchard

Anselm

et al. 2019

Preprint

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The centromere is an essential chromosomal region required for accurate chromosome segregation.Most eukaryotic centromeres are defined epigenetically by the histone H3 variant, CENP-A, yet how its self-propagation is achieved remains poorly understood. Here we developed a heterologous system to reconstitute epigenetic inheritance of centromeric chromatin by ectopically targeting the Drosophila centromere proteins dCENP-A, dCENP-C and CAL1 to LacO arrays in human cells. Dissecting the function of these three components uncovers the key role of self-association of dCENP-C and CAL1 for their mutual interaction and dCENP-A deposition. Importantly, we identify the components required for dCENP-C loading onto chromatin, involving a cooperation between CAL1 and dCENP-A nucleosomes, thus closing the epigenetic loop to ensure dCENP-C and dCENP-A replenishment during the cell division cycle. Finally, we show that all three Drosophila factors are sufficient for dCENP-A propagation and propose a model for the epigenetic inheritance of centromere identity.

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Section: Discussionmentioning

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Epigenetic inheritance of centromere identity in a heterologous system

Roure

Medina‐Pritchard

Anselm

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…For example, CAL1 also interacts with the highly conserved FACT complex (Chen et al, 2015) and localizes to the nucleolus (Chen et al, 2012; Lidsky et al, 2013). We hypothesize that the overall CAL1 sequence is under purifying selection (Phansalkar et al, 2012) to preserve its functional interactions with highly conserved partners, while key residues within the N terminus of CAL1 evolve to maintain the functional interaction with CENP-A.…”

Section: Discussionmentioning

confidence: 99%

Co-evolving CENP-A and CAL1 Domains Mediate Centromeric CENP-A Deposition across Drosophila Species

Rosin

Mellone

2016

Developmental Cell

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SUMMARY Centromeres mediate the conserved process of chromosome segregation, yet centromeric DNA and the centromeric histone, CENP-A, are rapidly evolving. The rapid evolution of Drosophila CENP-A loop 1 (L1) is thought to modulate the DNA-binding preferences of CENP-A to counteract centromere drive, the preferential transmission of chromosomes with expanded centromeric satellites. Consistent with this model, CENP-A from Drosophila bipectinata (bip) cannot localize to Drosophila melanogaster (mel) centromeres. We show that this result is due to the inability of the mel CENP-A chaperone, CAL1, to deposit bip CENP-A into chromatin. Co-expression of bip CENP-A and bip CAL1 in mel cells restores centromeric localization, and similar findings apply to other Drosophila species. We identify two co-evolving regions, CENP-A L1 and the CAL1 N terminus, as critical for lineage-specific CENP-A incorporation. Collectively, our data show that the rapid evolution of L1 modulates CAL1-mediated CENP-A assembly, suggesting an alternative mechanism for the suppression of centromere drive.

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“…Unlike canonical chromatin maintenance, centromeric chromatin maintenance is decoupled from DNA replication. As a result, CENP-A levels on the sister chromatids are reduced by half during replication (Jansen et al, 2007;Hemmerich et al, 2008;Dunleavy et al, 2009;Mellone et al, 2011;Lidsky et al, 2013). To ensure stable centromere maintenance, CENP-A nucleosomes must return to their original levels through active CENP-A deposition.…”

Section: Introductionmentioning

confidence: 99%

Structural basis for centromere maintenance by Drosophila CENP ‐A chaperone CAL 1

et al. 2020

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Centromeres are microtubule attachment sites on chromosomes defined by the enrichment of histone variant CENP‐A‐containing nucleosomes. To preserve centromere identity, CENP‐A must be escorted to centromeres by a CENP‐A‐specific chaperone for deposition. Despite this essential requirement, many eukaryotes differ in the composition of players involved in centromere maintenance, highlighting the plasticity of this process. In humans, CENP‐A recognition and centromere targeting are achieved by HJURP and the Mis18 complex, respectively. Using X‐ray crystallography, we here show how Drosophila CAL1, an evolutionarily distinct CENP‐A histone chaperone, binds both CENP‐A and the centromere receptor CENP‐C without the requirement for the Mis18 complex. While an N‐terminal CAL1 fragment wraps around CENP‐A/H4 through multiple physical contacts, a C‐terminal CAL1 fragment directly binds a CENP‐C cupin domain dimer. Although divergent at the primary structure level, CAL1 thus binds CENP‐A/H4 using evolutionarily conserved and adaptive structural principles. The CAL1 binding site on CENP‐C is strategically positioned near the cupin dimerisation interface, restricting binding to just one CAL1 molecule per CENP‐C dimer. Overall, by demonstrating how CAL1 binds CENP‐A/H4 and CENP‐C, we provide key insights into the minimalistic principles underlying centromere maintenance.

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Distinct modes of centromere protein dynamics during cell cycle progression in Drosophila S2R+ cells

Cited by 31 publications

References 83 publications

Epigenetic inheritance of centromere identity in a heterologous system

Epigenetic inheritance of centromere identity in a heterologous system

Co-evolving CENP-A and CAL1 Domains Mediate Centromeric CENP-A Deposition across Drosophila Species

Structural basis for centromere maintenance by Drosophila CENP ‐A chaperone CAL 1

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