Acetylation of Smc3 by Eco1 Is Required for S Phase Sister Chromatid Cohesion in Both Human and Yeast

Zhang, Jinglan; Shi, Xinling; Li, Yehua; Kim, Beom-Jun; Jia, Junling; Huang, Zhiwei; Yang, Tao; Fu, Xiaoyong; Jung, Sung Yun; Wang, Yi; Zhang, Pumin; Kim, Seong-Tae; Pan, Xuewen; Qin, Jun

doi:10.1016/j.molcel.2008.06.006

Cited by 384 publications

(425 citation statements)

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“…Early studies had pointed out the involvement of a specialized class of acetyltransferases (Eco1/Ctf7 in budding yeast; ESCO1 and ESCO2 in vertebrates) (Ivanov et al 2002;Bellows et al 2003). A series of subsequent studies showed that two conserved residues in SMC3 are the essential targets of the Eco1/ESCO1 acetyltransferase, and the acetylation reactions are indeed essential for cohesion establishment in budding yeast (Ben-Shahar et al 2008;Unal et al 2008) and humans (Zhang et al 2008). More recently, the deacetylase that reverses this reaction has been identified as Hos1 in budding yeast (Beckouët et al 2010;Borges et al 2010;Xiong et al 2010) and HDAC8 in humans (Deardorff et al 2012).…”

Section: Cohesin Establishes Sister Chromatid Cohesion During S Phasementioning

confidence: 99%

Chromosome Dynamics during Mitosis

Hirano

2015

Cold Spring Harb Perspect Biol

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The primary goal of mitosis is to partition duplicated chromosomes into daughter cells. Eukaryotic chromosomes are equipped with two distinct classes of intrinsic machineries, cohesin and condensins, that ensure their faithful segregation during mitosis. Cohesin holds sister chromatids together immediately after their synthesis during S phase until the establishment of bipolar attachments to the mitotic spindle in metaphase. Condensins, on the other hand, attempt to "resolve" sister chromatids by counteracting cohesin. The products of the balancing acts of cohesin and condensins are metaphase chromosomes, in which two rod-shaped chromatids are connected primarily at the centromere. In anaphase, this connection is released by the action of separase that proteolytically cleaves the remaining population of cohesin. Recent studies uncover how this series of events might be mechanistically coupled with each other and intricately regulated by a number of regulatory factors.

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Section: Cohesin Establishes Sister Chromatid Cohesion During S Phasementioning

confidence: 99%

Chromosome Dynamics during Mitosis

Hirano

2015

Cold Spring Harb Perspect Biol

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“…An antiestablishment complex consisting of Wings Apart-Like protein (WAPL)/Rad61 and Pds5 is required to maintain cohesion during G2/M by stabilizing the interaction between cohesin and the chromosomes (Panizza et al, 2000;Losada et al, 2005;Gandhi et al, 2006). While the specific details of how Ctf7, WAPL/Rad61, and Pds5 function together to first establish and then maintain cohesion still need to be clarified, recent results indicate that Ctf7 acetylates conserved Lys residues in SMC3, which inhibits the antiestablishment function of the Wpl1-Pds5 complex and promotes cohesion establishment (Ben-Shahar et al, 2008;Unal et al, 2008;Zhang et al, 2008;Rowland et al, 2009;Sutani et al, 2009). Ctf7 is also involved in the postreplicative induction of cohesion induced by DNA double-strand breaks (Unal et al, 2007).…”

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confidence: 99%

Proper Levels of the Arabidopsis Cohesion Establishment Factor CTF7 Are Essential for Embryo and Megagametophyte, But Not Endosperm, Development

Jiang

Xia

et al. 2010

Plant Physiology

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CTF7 is an essential gene in yeast that is required for the formation of sister chromatid cohesion. While recent studies have provided insights into how sister chromatid cohesion is established, less is known about how specifically CTF7 facilitates the formation of cohesion, and essentially nothing is known about how sister chromatid cohesion is established in plants. In this report, we describe the isolation and characterization of CTF7 from Arabidopsis (Arabidopsis thaliana). Arabidopsis CTF7 is similar to Saccharomyces cerevisiae CTF7 in that it lacks an amino-terminal extension, exhibits acetyltransferase activity, and can complement a yeast ctf7 temperature-sensitive mutation. CTF7 transcripts are found throughout the plant, with the highest levels present in buds. Seeds containing T-DNA insertions in CTF7 exhibit mitotic defects in the zygote. Interestingly, the endosperm developed normally in ctf7 seeds, suggesting that CTF7 is not essential for mitosis in endosperm nuclei. Minor defects were observed in female gametophytes of ctf7 1/2 plants, and plants that overexpress CTF7 exhibited female gametophyte lethality. Pollen development appeared normal in both CTF7 knockout and overexpression plants. Therefore, proper levels of CTF7 are critical for female gametophyte and embryo development but not for the establishment of mitotic cohesion during microgametogenesis or during endosperm development.The proper formation of sister chromatid cohesion and its subsequent release at the metaphase-to-anaphase transition is essential for the proper segregation of genetic material during cell division. It is critical for the compaction of chromosomes and their bipolar attachment to the spindle, DNA double-strand break repair, and the regulation of gene expression (for review, see Nasmyth and Haering, 2009). Sister chromatid cohesion is controlled by the cohesin complex, which consists of a heterodimer of Structural Maintenance of Chromosome (SMC) proteins, SMC1 and SMC3, Sister Chromatid Cohesion (SCC) protein SCC3, and SCC1, an a-kleisin protein. Perhaps the most widely accepted model of how cohesin functions has been referred to as the ring model, where the cohesin ring encircles the replicated sisters, holding them together until SCC1 cleavage by separase at the metaphase-to-anaphase transition opens the ring, allowing the release of the sister chromatids (for review, see Nasmyth and Haering, 2009).

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“…wapl1-1 wapl2 plants appear relatively normal but exhibit defects in both male and female meiosis (De et al, 2014). Also similar to the situation in yeast (Rolef Ben-Shahar et al, 2008;Unal et al, 2008;Zhang et al, 2008;Rowland et al, 2009;Sutani et al, 2009), inactivation of WAPL suppresses the lethality associated with ctf7 mutations in Arabidopsis (De et al, 2014). wapl1-1 wapl2 ctf7 plants are obtained at expected rates, display normal growth and development, and produce small numbers of viable seed.…”

Section: Discussionmentioning

confidence: 66%

“…Prior to S phase, cohesin binding to the chromosomes is dynamic and is regulated by a complex containing the Wings apart-like (Wapl) and Precocious Dissociation of Sisters 5 (Pds5) proteins, which have been termed the releasing or antiestablishment complexes (Gandhi et al, 2006;Gerlich et al, 2006;Kueng et al, 2006;Rolef Ben-Shahar et al, 2008;Rowland et al, 2009;Sutani et al, 2009;Ouyang et al, 2013). The establishment of cohesion, which occurs during S phase (Skibbens et al, 1999;Tóth et al, 1999), is facilitated by acetylation of two adjacent lysine residues on SMC3 by the Ctf7 (Chromosome Transmission Fidelity7)/Eco1 acetyltransferase (Rolef Ben-Shahar et al, 2008;Unal et al, 2008;Zhang et al, 2008;Rowland et al, 2009). This modification of the cohesin complex appears to antagonize the action of the Wapl-Pds5 complex and to stabilize the association of cohesin with the chromatin (Rolef Ben-Shahar et al, 2008;Unal et al, 2008;Zhang et al, 2008;Rowland et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…The establishment of cohesion, which occurs during S phase (Skibbens et al, 1999;Tóth et al, 1999), is facilitated by acetylation of two adjacent lysine residues on SMC3 by the Ctf7 (Chromosome Transmission Fidelity7)/Eco1 acetyltransferase (Rolef Ben-Shahar et al, 2008;Unal et al, 2008;Zhang et al, 2008;Rowland et al, 2009). This modification of the cohesin complex appears to antagonize the action of the Wapl-Pds5 complex and to stabilize the association of cohesin with the chromatin (Rolef Ben-Shahar et al, 2008;Unal et al, 2008;Zhang et al, 2008;Rowland et al, 2009). In animal cells, acetylation of SMC3 facilitates the recruitment of sororin and displacement of Wapl to help create a stable cohesin complex (Lafont et al, 2010;Nishiyama et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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The Opposing Actions of Arabidopsis CHROMOSOME TRANSMISSION FIDELITY7 and WINGS APART-LIKE1 and 2 Differ in Mitotic and Meiotic Cells

Bolaños-Villegas

Mitra

et al. 2016

Plant Cell

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Sister chromatid cohesion, which is mediated by the cohesin complex, is essential for the proper segregation of chromosomes during mitosis and meiosis. Stable binding of cohesin with chromosomes is regulated in part by the opposing actions of CTF7 (CHROMOSOME TRANSMISSION FIDELITY7) and WAPL (WINGS APART-LIKE). In this study, we characterized the interaction between Arabidopsis thaliana CTF7 and WAPL by conducting a detailed analysis of wapl1-1 wapl2 ctf7 plants. ctf7 plants exhibit major defects in vegetative growth and development and are completely sterile. Inactivation of WAPL restores normal growth, mitosis, and some fertility to ctf7 plants. This shows that the CTF7/WAPL cohesin system is not essential for mitosis in vegetative cells and suggests that plants may contain a second mechanism to regulate mitotic cohesin. WAPL inactivation restores cohesin binding and suppresses ctf7-associated meiotic cohesion defects, demonstrating that WAPL and CTF7 function as antagonists to regulate meiotic sister chromatid cohesion. The ctf7 mutation only had a minor effect on wapl-associated defects in chromosome condensation and centromere association. These results demonstrate that WAPL has additional roles that are independent of its role in regulating chromatin-bound cohesin.

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Acetylation of Smc3 by Eco1 Is Required for S Phase Sister Chromatid Cohesion in Both Human and Yeast

Cited by 384 publications

References 17 publications

Chromosome Dynamics during Mitosis

Chromosome Dynamics during Mitosis

Proper Levels of the Arabidopsis Cohesion Establishment Factor CTF7 Are Essential for Embryo and Megagametophyte, But Not Endosperm, Development

The Opposing Actions of Arabidopsis CHROMOSOME TRANSMISSION FIDELITY7 and WINGS APART-LIKE1 and 2 Differ in Mitotic and Meiotic Cells

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