APC/C-Cdc20 mediates deprotection of centromeric cohesin at meiosis II in yeast

Jonak, Katarzyna; Zagoriy, Ievgeniia; Oz, Tugce; Graf, Peter; Rojas, Julie; Mengoli, Valentina; Zachariae, Wolfgang

doi:10.1080/15384101.2017.1320628

Cited by 26 publications

(34 citation statements)

References 61 publications

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“…Equally mysterious is the mechanism by which protection of peri-centromeric cohesin from separase is lost by the time cells initiate anaphase II. In budding yeast, degradation by APC/C Cdc20 of its sole shugoshin ortholog Sgo1 at the onset of anaphase II, a phenomenon that does not occur at the equivalent stage of meiosis I, ensures that Sgo1 and PP2A are removed by the time separase is activated (Jonak et al, 2017). However, SGOL2, which confers protection during meiosis I in mammals, does not possess this regulatory feature (Marston, 2015).…”

Section: Introductionmentioning

confidence: 99%

Loss of Sister Kinetochore Co-orientation and Peri-centromeric Cohesin Protection after Meiosis I Depends on Cleavage of Centromeric REC8

Ogushi

Rattani

Godwin

et al. 2020

Preprint

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2 Summary Protection of peri-centromeric REC8 cohesin from separase and sister kinetochore attachment to microtubules emanating from the same spindle pole (co-orientation) ensure that sister chromatids remain associated after meiosis I. Both features are lost during meiosis II, when sister kinetochores bi-orient and lose peri-centromeric REC8 protection, resulting in sister chromatid disjunction and the production of haploid gametes. By transferring spindle-chromosome complexes (SCCs) between meiosis I and II cells, we have discovered that both sister kinetochore co-orientation and pericentromeric cohesin protection depend on the SCC and not the cytoplasm. Moreover, the catalytic activity of separase at meiosis I is necessary not only for converting kinetochores from a co-to a bi-oriented state but also for deprotection of pericentromeric cohesin and that cleavage of REC8 may be the key event. Crucially, we show that selective cleavage of REC8 in the vicinity of kinetochores is sufficient to destroy co-orientation in univalent chromosomes, albeit not in bivalents where resolution of chiasmata through cleavage of Rec8 along chromosome arms may also be required. 65the fission yeast S.pombe (Gregan et al., 2008) and indeed is absent from metazoan 66 genomes (Plowman et al., 2019), some other mechanism must confer co-orientation in 67 eukaryotes with regional centromeres. In fission yeast, a meiosis-specific version of 68 cohesin containing a Rec8 kleisin subunit is necessary to prevent bi-orientation during 69 meiosis I (Watanabe and Nurse, 1999; Sakuno et al, 2009). This suggests that cohesin 70 5 mediates co-orientation by holding sister centromeres together. Though plausible, this 71 hypothesis has never been rigorously proven. In an attempt to target specifically the 72 centromeric cohesin population for cleavage using fission yeast strains expressing a 73 CenpC-TEV fusion and Rec8 containing TEV sites, there was little or no evidence that 74 centromeric cohesin was more depleted than peri-centromeric cohesin (Yokobayashi & 75 Watanabe, 2005). 77Another important meiotic regulatory factor both in fungi and metazoa is a family of 78 proteins related to Spo13 in budding yeast (Wang et al., 1987). These include Moa1 in 79 fission yeast (Yokobayashi & Watanabe, 2005) and Meikin (Kim et al., 2015) in 80 mammals. Though not highly conserved in amino-acid sequences, all members of the 81 family are expressed exclusively during meiosis and have the property of recruiting 82 Polo-like kinases to kinetochores. Because their ablation compromises protection of 83 peri-centromeric cohesion by Shugoshin/Mei-S332 proteins (Katis et al., 2004a;84 Klapholz & Esposito, 1980; Lee et al., 2004; Shonn et al., 2002) and regulation of the 85 anaphase-promoting complex/cyclosome (APC/C) activity (Katis et al., 2004b) as well 86 as co-orientation (Galander et al., 2019; Kim et al., 2015; Matos et al., 2008; Miyazaki 87 et al., 2017), these Spo13-like proteins should be viewed as factors that regulate 88 directly or indirectly numerous...

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Section: Introductionmentioning

confidence: 99%

Loss of Sister Kinetochore Co-orientation and Peri-centromeric Cohesin Protection after Meiosis I Depends on Cleavage of Centromeric REC8

Ogushi

Rattani

Godwin

et al. 2020

Preprint

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“…Similar to mitosis, the centromeric localization of Sgo1 during meiosis also depends on Bub1-mediated phosphorylation of H2A [91]. The activation of ubiquitin-ligase APC/C-Cdc20 removes PP2A Rts1 from centromeres by targeting Sgo1 for degradation, which leads to Rec8 phosphorylation and cleavage in meiotic anaphase II [122]. In addition, Sgo1 recruits Ipl1 to kinetochores during meiosis, which maintains PP2A Rts1 activity at centromeres [123].…”

Section: The Function Of Phosphatases In Meiosismentioning

confidence: 99%

The Opposing Functions of Protein Kinases and Phosphatases in Chromosome Bipolar Attachment

Sherwin

Wang

2019

IJMS

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Accurate chromosome segregation during cell division is essential to maintain genome integrity in all eukaryotic cells, and chromosome missegregation leads to aneuploidy and therefore represents a hallmark of many cancers. Accurate segregation requires sister kinetochores to attach to microtubules emanating from opposite spindle poles, known as bipolar attachment or biorientation. Recent studies have uncovered several mechanisms critical to chromosome bipolar attachment. First, a mechanism exists to ensure that the conformation of sister centromeres is biased toward bipolar attachment. Second, the phosphorylation of some kinetochore proteins destabilizes kinetochore attachment to facilitate error correction, but a protein phosphatase reverses this phosphorylation. Moreover, the activity of the spindle assembly checkpoint is regulated by kinases and phosphatases at the kinetochore, and this checkpoint prevents anaphase entry in response to faulty kinetochore attachment. The fine-tuned kinase/phosphatase balance at kinetochores is crucial for faithful chromosome segregation during both mitosis and meiosis. Here, we discuss the function and regulation of protein phosphatases in the establishment of chromosome bipolar attachment with a focus on the model organism budding yeast.

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“…In agreement with this model also applying in higher eukaryotes, inhibition of PP2A-B56 activity, or loss of Sgo2 (which is required for PP2A-B56 recruitment in higher eukaryotes) during the first meiotic division lead to cleavage of Rec8 not only on chromosome arms but also in the centromere region, and hence, precocious sister chromatid separation already in meiosis I (Chang et al, 2011;Lee et al, 2008;Llano et al, 2008;Mailhes et al, 2003;Rattani et al, 2013). Nevertheless, it is still unknown how protection of centromeric cohesin is removed in meiosis II only (a process also called "deprotection" (Chambon et al, 2013b;Jonak et al, 2017;Wassmann, 2013), to allow separation of sister chromatids.…”

Section: Introductionmentioning

confidence: 99%

“…First, bipolar tension applied on sister kinetochores in meiosis II, but not meiosis I, was suggested to move Sgo2-PP2A-B56 far enough away from Rec8 to allow its phosphorylation (Gomez et al, 2007;Lee et al, 2008). Second, degradation of Sgo1 and Mps1 at anaphase II onset in an APC/C-dependent manner was proposed to ensure deprotection in budding yeast (Jonak et al, 2017). Third, using a Morpholino-knockdown approach we proposed that I2PP2A/Set, a Histone chaperone and potential PP2A inhibitor, counteracts protection of Rec8 specifically in meiosis II in a tension-independent manner (Chambon et al, 2013b).…”

Section: Introductionmentioning

confidence: 99%

Kinetochore individualization in meiosis I is required for centromeric cohesin removal in meiosis II

Gryaznova

Keating

Touati

et al. 2020

Preprint

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Partitioning of the genome in meiosis occurs through two highly specialized cell divisions, named meiosis I and II. Step-wise cohesin removal is required for chromosome segregation in meiosis I, and sister chromatid segregation in meiosis II. In meiosis I, mono-oriented sister kinetochores appear as fused together when examined by high resolution confocal microscopy, whereas they are clearly separated in meiosis II, when attachments are bipolar. It has been proposed that bipolar tension applied by the spindle is responsible for the physical separation of sister kinetochores, removal of cohesin protection and chromatid separation in meiosis II. We show here that this is not the case, and initial separation of sister kinetochores occurs already in anaphase I, when attachments are still monopolar, and independently of pericentromeric Sgo2 removal. This kinetochore individualization occurs also independently of spindle forces applied on sister kinetochores, but importantly, depends on cleavage activity of Separase. Crucially, without kinetochore individualization by Separase in meiosis I, oocytes separate bivalents into chromosomes and not sister chromatids in meiosis II, showing that whether centromeric cohesin is removed or not is determined by the kinetochore structure prior to meiosis II.

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APC/C-Cdc20 mediates deprotection of centromeric cohesin at meiosis II in yeast

Cited by 26 publications

References 61 publications

Loss of Sister Kinetochore Co-orientation and Peri-centromeric Cohesin Protection after Meiosis I Depends on Cleavage of Centromeric REC8

Loss of Sister Kinetochore Co-orientation and Peri-centromeric Cohesin Protection after Meiosis I Depends on Cleavage of Centromeric REC8

The Opposing Functions of Protein Kinases and Phosphatases in Chromosome Bipolar Attachment

Kinetochore individualization in meiosis I is required for centromeric cohesin removal in meiosis II

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