Budding Yeast Wpl1(Rad61)-Pds5 Complex Counteracts Sister Chromatid Cohesion-Establishing Reaction

Sutani, Takashi; Kawaguchi, Takashi; Kanno, Ryuhi; Itoh, Takehiko; Shirahige, Katsuhiko

doi:10.1016/j.cub.2009.01.062

Cited by 204 publications

(310 citation statements)

References 34 publications

(61 reference statements)

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“…First, whereas yeast cohesin is loaded during S-phase, its human counterpart is loaded in telophase; second, yeast cohesin is enriched within intergenic regions between convergent transcripts, most of human cohesin colocalizes with CTCF, a zinc-finger protein required for transcriptional insulation (26,28,31); third, a functional divergence has been observed with WAPL, which seems to play an exclusively negative role in regulating cohesion in human and fission yeast but both positive and negative roles in budding yeast (39,(42)(43)(44)(45). Thus, whereas cohesion reinforcement is a conserved biological process used by both yeast and human, the molecular details appear to be different in that distinct cohesin subunit is targeted in response to DNA damage.…”

Section: The Biological Process Of Cohesion Reinforcement Is Conservementioning

confidence: 99%

Genome-wide Reinforcement of Cohesin Binding at Pre-existing Cohesin Sites in Response to Ionizing Radiation in Human Cells

Kim

Zhang

et al. 2010

Journal of Biological Chemistry

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The cohesin complex plays a central role in genome maintenance by regulation of chromosome segregation in mitosis and DNA damage response (DDR) in other phases of the cell cycle. The ATM/ATR phosphorylates SMC1 and SMC3, two core components of the cohesin complex to regulate checkpoint signaling and DNA repair. In this report, we show that the genomewide binding of SMC1 and SMC3 after ionizing radiation (IR) is enhanced by reinforcing pre-existing cohesin binding sites in human cancer cells. We demonstrate that ATM and SMC3 phosphorylation at Ser 1083 regulate this process. We also demonstrate that acetylation of SMC3 at Lys 105 and Lys 106 is induced by IR and this induction depends on the acetyltransferase ESCO1 as well as the ATM/ATR kinases. Consistently, both ESCO1 and SMC3 acetylation are required for intra-S phase checkpoint and cellular survival after IR. Although both IR-induced acetylation and phosphorylation of SMC3 are under the control of ATM/ATR, the two forms of modification are independent of each other and both are required to promote reinforcement of SMC3 binding to cohesin sites. Thus, SMC3 modifications is a mechanism for genome-wide reinforcement of cohesin binding in response to DNA damage response in human cells and enhanced cohesion is a downstream event of DDR.Sister chromatid cohesion is a fundamental biological process that the sister chromatids once generated in S-phase are always paired and linked to ensure equal distribution to daughter cells until mitosis. Cohesion plays a central role in genome stability by facilitating spindle bi-orientation, faithful chromosome segregation, homologous recombination, checkpoint activation, and transcriptional regulation (1-3). This process is mediated by a protein complex called cohesin that consists of four core subunits SMC1, SMC3, RAD21 (also known as SCC1 and MCD1), and SA2/SA1 (also known as SCC3, or STAG2 and STAG1) and several accessory factors (4).To maintain the fidelity of the genome, cells evolve with an elaborate mechanism to deal with DNA damage. DNA damage response (DDR) 3 is a signal transduction pathway that coordinates cell cycle arrest, DNA repair, and programmed cell death in the presence of damaged DNA (5, 6). It is regulated by the ATM/ATR, master regulators of the DDR process through phosphorylation of their substrates (6 -10). Disruption of DDR results in genomic instability and is the cause for many cancerprone disorders (11). Cohesin is an important effector in the DNA damage response. SMC1 and SMC3 are phosphorylated in human and mouse cells in an ATM/ATR-dependent manner and these phosphorylation events are required for intra-S checkpoint, cellular survival in response to IR (12-15). Cohesin is recruited to sites of DNA damage for efficient DNA repair (4,12,16,17). However, the molecular mechanism by which cohesin phosphorylation regulates DDR is still unknown.Acetylation is another post-translational modification mechanism for the regulation of cohesin functions. It has been long recognized that Eco1 (establishment o...

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Section: The Biological Process Of Cohesion Reinforcement Is Conservementioning

confidence: 99%

Genome-wide Reinforcement of Cohesin Binding at Pre-existing Cohesin Sites in Response to Ionizing Radiation in Human Cells

Kim

Zhang

et al. 2010

Journal of Biological Chemistry

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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).…”

mentioning

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%

“…Studies in yeast and animal cells have shown that WAPL in conjunction with PDS5 plays an important role in regulating the reversible binding of cohesin to chromosomes (Bernard et al, 2008;Sutani et al, 2009;Chan et al, 2012;LopezSerra et al, 2013). Prior to DNA replication, WAPL either opens or maintains an open conformation of the cohesin ring at the junction between the SMC3 ATPase domain and the SCC1 N-terminal WHD (Chatterjee et al, 2013;Ouyang et al, 2013).…”

Section: Proper Cohesin Levels Are Essential For Meiotic Chromosome Smentioning

confidence: 99%

“…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).…”

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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Budding Yeast Wpl1(Rad61)-Pds5 Complex Counteracts Sister Chromatid Cohesion-Establishing Reaction

Cited by 204 publications

References 34 publications

Genome-wide Reinforcement of Cohesin Binding at Pre-existing Cohesin Sites in Response to Ionizing Radiation in Human Cells

Genome-wide Reinforcement of Cohesin Binding at Pre-existing Cohesin Sites in Response to Ionizing Radiation in Human Cells

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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