Esco1 Acetylates Cohesin via a Mechanism Different from That of Esco2

Minamino, Masashi; Ishibashi, Mai; Nakato, Ryuichiro; Akiyama, Kazuhiro; Tanaka, Hiroshi; Kato, Yuki; Negishi, Lumi; Hirota, Toru; Sutani, Takashi; Bando, Masashige; Shirahige, Katsuhiko

doi:10.1016/j.cub.2015.05.017

Cited by 75 publications

(110 citation statements)

References 43 publications

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“…First, we discovered that Esco1 is selectively and ubiquitously recruited by cohesin, and moreover occupies its binding sites throughout the cell cycle. Comparable observations were made by Minamino et al and reported during revision of this study (46). Second, we found that depleting either Esco1 or cohesin had similar effects on transcription, mainly involving the up-regulation of Esco1-proximal genes.…”

Section: Discussionsupporting

confidence: 90%

Cohesin recruits the Esco1 acetyltransferase genome wide to repress transcription and promote cohesion in somatic cells

Rahman

Jallepalli

2015

Proc. Natl. Acad. Sci. U.S.A.

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The cohesin complex links DNA molecules and plays key roles in the organization, expression, repair, and segregation of eukaryotic genomes. In vertebrates the Esco1 and Esco2 acetyltransferases both modify cohesin's Smc3 subunit to establish sister chromatid cohesion during S phase, but differ in their N-terminal domains and expression during development and across the cell cycle. Here we show that Esco1 and Esco2 also differ dramatically in their interaction with chromatin, as Esco1 is recruited by cohesin to over 11,000 sites, whereas Esco2 is infrequently enriched at REST/NRSF target genes. Esco1's colocalization with cohesin occurs throughout the cell cycle and depends on two short motifs (the A-box and B-box) present in and unique to all Esco1 orthologs. Deleting either motif led to the derepression of Esco1-proximal genes and functional uncoupling of cohesion from Smc3 acetylation. In contrast, other mutations that preserved Esco1's recruitment separated its roles in cohesion establishment and gene silencing. We conclude that Esco1 uses cohesin as both a substrate and a scaffold for coordinating multiple chromatinbased transactions in somatic cells. mitosis | gene expression | sister chromatids | chromosomes | acetylation

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Section: Discussionsupporting

confidence: 90%

Cohesin recruits the Esco1 acetyltransferase genome wide to repress transcription and promote cohesion in somatic cells

Rahman

Jallepalli

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Both ESCO1 and ESCO2 can acetylate SMC3 at K105 and K106, although ESCO1 can acetylate cohesin independently of DNA replication (Minamino et al 2015). The roles of vertebrate ESCO1, ESCO2, and SMC3 acetylation and their functional interplay in different processes related to proliferation have not been addressed to date, one of the reasons likely being related to the technical challenges of conditionally and concomitantly mutating/inactivating multiple genes in vertebrate cells.…”

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confidence: 99%

ESCO1/2's roles in chromosome structure and interphase chromatin organization

et al. 2017

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ESCO1/2 acetyltransferases mediating SMC3 acetylation and sister chromatid cohesion (SCC) are differentially required for genome integrity and development. Here we established chicken DT40 cell lines with mutations in ESCO1/2, SMC3 acetylation, and the cohesin remover WAPL. Both ESCO1 and ESCO2 promoted SCC, while ESCO2 was additionally and specifically required for proliferation and centromere integrity. ESCO1 overexpression fully suppressed the slow proliferation and centromeric separation phenotypes of esco2 cells but only partly suppressed its chromosome arm SCC defects. Concomitant inactivation of ESCO1 and ESCO2 caused lethality owing to compromised mitotic chromosome segregation. Neither wapl nor acetyl-mimicking smc3-QQ mutations rescued esco1 esco2 lethality. Notably, esco1 esco2 wapl conditional mutants showed very severe proliferation defects associated with catastrophic mitoses and also abnormal interphase chromatin organization patterns. The results indicate that cohesion establishment by vertebrate ESCO1/2 is linked to interphase chromatin architecture formation, a newly identified function of cohesin acetyltransferases that is both fundamentally and medically relevant.

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“…Pds5A-and Pds5B-deficient mice have developmental abnormalities [63,64], and both Pds5A and Pds5B are shown to contribute to sister chromatid cohesion in mouse cells [63]. In human cells, Pds5 is required for Smc3 acetylation [65], suggesting that it should be required for cohesion establishment. However, only mild or no cohesion defects were observed in Pds5A and Pds5B-depleted human cells [59,65], possibly due to incomplete depletion and the dual roles of Pds5 in both cohesion establishment and resolution.…”

Section: Cohesin-associated Regulatorsmentioning

confidence: 99%

“…In human cells, Pds5 is required for Smc3 acetylation [65], suggesting that it should be required for cohesion establishment. However, only mild or no cohesion defects were observed in Pds5A and Pds5B-depleted human cells [59,65], possibly due to incomplete depletion and the dual roles of Pds5 in both cohesion establishment and resolution. Further studies, such as in vitro biochemical reconstitution and structural analysis, are required to more clearly define the functions of Pds5 in sister chromatid cohesion.…”

Section: Cohesin-associated Regulatorsmentioning

confidence: 99%

“…Indeed, cohesin acetylation can occur efficiently before and after DNA replication in Xenopus egg extracts [91]. In human cells, Esco1 has been shown to constitutively co-localize with and mediate the acetylation of cohesin at CTCF sites throughout the cell cycle [65,92]. This replication-independent cohesin acetylation mediates gene silencing [92].…”

Section: Establishment Of Sister Chromatid Cohesionmentioning

confidence: 99%

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Regulation of sister chromatid cohesion during the mitotic cell cycle

2015

Sci. China Life Sci.

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Orderly execution of two critical events during the cell cycle--DNA replication and chromosome segregation--ensures the stable transmission of genetic materials. The cohesin complex physically connects sister chromatids during DNA replication in a process termed sister chromatid cohesion. Timely establishment and dissolution of sister chromatid cohesion is a prerequisite for accurate chromosome segregation, and is tight regulated by the cell cycle machinery and cohesin-associated proteins. In this review, we discuss recent progress in the molecular understanding of sister chromatid cohesion during the mitotic cell cycle.cell cycle, mitosis, sister chromatid cohesion, cohesin, cohesin loading, cohesin release, DNA replication, cohesion establishment Citation:Zheng G, Yu HT. Regulation of sister chromatid cohesion during the mitotic cell cycle. Sci China Life Sci, 2015Sci, , 58: 1089Sci, -1098Sci, , doi: 10.1007 During the cell cycle, DNA undergoes replication during S phase to generate two identical copies of each chromosome, called sister chromatids. During mitosis, sister chromatids are separated and partitioned evenly to the two daughter cells to maintain genomic stability. Cells receive too many or too few chromosomes become aneuploid. Aneuploidy can drive tumorigenesis in a context-dependent manner [1,2]. To prevent premature sister chromatid separation and ensure accurate chromosome segregation, sister chromatids are physically tethered to each other through the process of sister chromatid cohesion, as well as DNA catenation, from S phase till metaphase. Sister chromatid cohesion is mediated by the highly conserved ring-shaped cohesin complex, which topologically entraps chromosomes [3,4]. Cohesion establishment, maintenance, and removal at different cell cycle phases require a series of coordinated interactions between cohesin and its regulators (Figure 1). Cohesin is loaded onto DNA by the cohesin loader complex Scc2-Scc4 in telophase and early G1 [57]. At this stage, the chromatin-bound cohesin is highly dynamic, and can be released from chromosomes by the cohesin releasing factor Wapl, with the help of the scaffold protein Pds5 [811]. During S phase, the replicated sister chromatids are tethered by cohesin to establish sister chromatid cohesion. Cohesion establishment requires the acetylation of two adjacent, evolutionarily conserved lysines on Smc3 by the acetyltransferase Eco1 (Esco1/2 in vertebrates) [1217], and in metazoans, the subsequent recruitment of sororin to cohesin through Pds5 [1821]. Smc3 acetylation and sororin antagonize the cohesin-releasing activity of Wapl-Pds5, thereby stabilizing cohesin on chromosomes [17,21]. Finally, in mitosis, cohesin is released from chromosomes in a stepwise manner in vertebrates [22]. In early mitosis, Pds5-bound sororin is phosphorylated by mitotic kinases and dissociates from cohesin [21,2325]. Sororin dissociation allows Wapl to gain access to Pds5 and cohesin, releasing cohesin from chromosome arms. At centromeres,

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Esco1 Acetylates Cohesin via a Mechanism Different from That of Esco2

Cited by 75 publications

References 43 publications

Cohesin recruits the Esco1 acetyltransferase genome wide to repress transcription and promote cohesion in somatic cells

Cohesin recruits the Esco1 acetyltransferase genome wide to repress transcription and promote cohesion in somatic cells

ESCO1/2's roles in chromosome structure and interphase chromatin organization

Regulation of sister chromatid cohesion during the mitotic cell cycle

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