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

References

• Nasmyth K. Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol 2011; 13:1170-7; PMID:21968990; https://doi.org/10.1038/ncb2349
   PubMed Web of Science ®Google Scholar
• Haarhuis JHI, Elbatsh AMO, Rowland BD. Cohesin and Its Regulation: On the Logic of X-Shaped Chromosomes. Developmental Cell 2014; 31:7-18; PMID:25313959; https://doi.org/10.1016/j.devcel.2014.09.010
   PubMed Web of Science ®Google Scholar
• Gligoris T, Lowe J. Structural Insights into Ring Formation of Cohesin and Related Smc Complexes. Trends Cell Biol 2016; 26:680-93; PMID:27134029; https://doi.org/10.1016/j.tcb.2016.04.002
   PubMed Web of Science ®Google Scholar
• He X, Asthana S, Sorger PK. Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 2000; 101:763-75; PMID:10892747; https://doi.org/10.1016/S0092-8674(00)80888-0
   PubMed Web of Science ®Google Scholar
• Musacchio A. The Molecular Biology of Spindle Assembly Checkpoint Signaling Dynamics. Curr Biol 2015; 25:R1002-18.
   PubMed Web of Science ®Google Scholar
• Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 2000; 103:375-86; PMID:11081625; https://doi.org/10.1016/S0092-8674(00)00130-6
   PubMed Web of Science ®Google Scholar
• Waizenegger IC, Hauf S, Meinke A, Peters JM. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 2000; 103:399-410; PMID:11081627; https://doi.org/10.1016/S0092-8674(00)00132-X
   PubMed Web of Science ®Google Scholar
• Petronczki M, Siomos MF, Nasmyth K. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 2003; 112:423-40; PMID:12600308; https://doi.org/10.1016/S0092-8674(03)00083-7
   PubMed Web of Science ®Google Scholar
• Hauf S, Watanabe Y. Kinetochore orientation in mitosis and meiosis. Cell 2004; 119:317-27; PMID:15507205; https://doi.org/10.1016/j.cell.2004.10.014
   PubMed Web of Science ®Google Scholar
• Nasmyth K. A meiotic mystery: How sister kinetochores avoid being pulled in opposite directions during the first division. Bioessays 2015; 37:657-65; PMID:25874377; https://doi.org/10.1002/bies.201500006
   PubMed Web of Science ®Google Scholar
• Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, Nasmyth K. Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 2000; 103:387-98; PMID:11081626; https://doi.org/10.1016/S0092-8674(00)00131-8
   PubMed Web of Science ®Google Scholar
• Terret ME, Wassmann K, Waizenegger I, Maro B, Peters JM, Verlhac MH. The meiosis I-to-meiosis II transition in mouse oocytes requires separase activity. Curr Biol 2003; 13:1797-802; PMID:14561405; https://doi.org/10.1016/j.cub.2003.09.032
   PubMed Web of Science ®Google Scholar
• Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, Xu H, Helmhart W, Kudo H, McKay M, Maro B, et al. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 2006; 126:135-46; PMID:16839882; https://doi.org/10.1016/j.cell.2006.05.033
   PubMed Web of Science ®Google Scholar
• Salah SM, Nasmyth K. Destruction of the securin Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 2000; 109:27-34; PMID:10855492; https://doi.org/10.1007/s004120050409
   PubMed Web of Science ®Google Scholar
• Kitajima TS, Miyazaki Y, Yamamoto M, Watanabe Y. Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. Embo J 2003; 22:5643-53; PMID:14532136; https://doi.org/10.1093/emboj/cdg527
   PubMed Web of Science ®Google Scholar
• Lee J, Okada K, Ogushi S, Miyano T, Miyake M, Yamashita M. Loss of Rec8 from chromosome arm and centromere region is required for homologous chromosome separation and sister chromatid separation, respectively, in mammalian meiosis. Cell Cycle 2006; 5:1448-55; PMID:16855401; https://doi.org/10.4161/cc.5.13.2903
   PubMed Web of Science ®Google Scholar
• Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 1999; 98:91-103; PMID:10412984; https://doi.org/10.1016/S0092-8674(00)80609-1
   PubMed Web of Science ®Google Scholar
• Watanabe Y, Nurse P. Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 1999; 400:461-4; PMID:10440376; https://doi.org/10.1038/22774
   PubMed Web of Science ®Google Scholar
• Toth A, Rabitsch KP, Galova M, Schleiffer A, Buonomo SB, Nasmyth K. Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 2000; 103:1155-68; PMID:11163190; https://doi.org/10.1016/S0092-8674(00)00217-8
   PubMed Web of Science ®Google Scholar
• Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 2001; 15:1349-60; PMID:11390355; https://doi.org/10.1101/gad.192701
   PubMed Web of Science ®Google Scholar
• Ishiguro T, Tanaka K, Sakuno T, Watanabe Y. Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 2010; 12:500-6; PMID:20383139; https://doi.org/10.1038/ncb2052
   PubMed Web of Science ®Google Scholar
• Katis VL, Lipp JJ, Imre R, Bogdanova A, Okaz E, Habermann B, Mechtler K, Nasmyth K, Zachariae W. Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 2010; 18:397-409; PMID:20230747; https://doi.org/10.1016/j.devcel.2010.01.014
   PubMed Web of Science ®Google Scholar
• Le AH, Mastro TL, Forsburg SL. The C-terminus of S. pombe DDK subunit Dfp1 is required for meiosis-specific transcription and cohesin cleavage. Biol Open 2013; 2:728-38.
   PubMed Web of Science ®Google Scholar
• Kerrebrock AW, Moore DP, Wu JS, Orr-Weaver TL. Mei-S332, a Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions. Cell 1995; 83:247-56; PMID:7585942; https://doi.org/10.1016/0092-8674(95)90166-3
   PubMed Web of Science ®Google Scholar
• Katis VL, Galova M, Rabitsch KP, Gregan J, Nasmyth K. Maintenance of cohesin at centromeres after meiosis I in budding yeast requires a kinetochore-associated protein related to MEI-S332. Curr Biol 2004; 14:560-72; PMID:15062096; https://doi.org/10.1016/j.cub.2004.03.001
   PubMed Web of Science ®Google Scholar
• Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 2004; 427:510-7; PMID:14730319; https://doi.org/10.1038/nature02312
   PubMed Web of Science ®Google Scholar
• Marston AL, Tham WH, Shah H, Amon A. A genome-wide screen identifies genes required for centromeric cohesion. Science 2004; 303:1367-70; PMID:14752166; https://doi.org/10.1126/science.1094220
   PubMed Web of Science ®Google Scholar
• Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K. Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 2004; 14:287-301; PMID:14972679; https://doi.org/10.1016/j.cub.2004.01.051
   PubMed Web of Science ®Google Scholar
• Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y. Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 2010; 327:172-7; PMID:19965387; https://doi.org/10.1126/science.1180189
   PubMed Web of Science ®Google Scholar
• Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 2006; 441:46-52; PMID:16541025; https://doi.org/10.1038/nature04663
   PubMed Web of Science ®Google Scholar
• Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 2006; 441:53-61; PMID:16541024; https://doi.org/10.1038/nature04664
   PubMed Web of Science ®Google Scholar
• Xu Z, Cetin B, Anger M, Cho US, Helmhart W, Nasmyth K, Xu W. Structure and function of the PP2A-shugoshin interaction. Mol Cell 2009; 35:426-41; PMID:19716788; https://doi.org/10.1016/j.molcel.2009.06.031
   PubMed Web of Science ®Google Scholar
• Gutierrez-Caballero C, Cebollero LR, Pendas AM. Shugoshins: from protectors of cohesion to versatile adaptors at the centromere. Trends Genet 2012; 28:351-60; PMID:22542109; https://doi.org/10.1016/j.tig.2012.03.003
   PubMed Web of Science ®Google Scholar
• Marston AL. Shugoshins: Tension-Sensitive Pericentromeric Adaptors Safeguarding Chromosome Segregation. Mol Cell Biol 2015; 35:634-48; PMID:25452306; https://doi.org/10.1128/MCB.01176-14
   PubMed Web of Science ®Google Scholar
• Clift D, Marston AL. The role of shugoshin in meiotic chromosome segregation. Cytogenet Genome Res 2011; 133:234-42; PMID:21273764; https://doi.org/10.1159/000323793
   PubMed Web of Science ®Google Scholar
• Llano E, Herran Y, Garcia-Tunon I, Gutierrez-Caballero C, de Alava E, Barbero JL, Schimenti J, de Rooij DG, Sanchez-Martin M, Pendas AM. Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol 2008; 197:877-85; https://doi.org/10.1083/jcb.201201100
   Web of Science ®Google Scholar
• Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y. Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 2008; 10:42-52; PMID:18084284; https://doi.org/10.1038/ncb1667
   PubMed Web of Science ®Google Scholar
• Petronczki M, Matos J, Mori S, Gregan J, Bogdanova A, Schwickart M, Mechtler K, Shirahige K, Zachariae W, Nasmyth K. Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 2006; 126:1049-64; PMID:16990132; https://doi.org/10.1016/j.cell.2006.07.029
   PubMed Web of Science ®Google Scholar
• Hirose Y, Suzuki R, Ohba T, Hinohara Y, Matsuhara H, Yoshida M, Itabashi Y, Murakami H, Yamamoto A. Chiasmata promote monopolar attachment of sister chromatids and their co-segregation toward the proper pole during meiosis I. PLoS Genet 2011; 7:e1001329; PMID:21423721; https://doi.org/10.1371/journal.pgen.1001329
   PubMed Web of Science ®Google Scholar
• Chambon JP, Touati SA, Berneau S, Cladiere D, Hebras C, Groeme R, McDougall A, Wassmann K. The PP2A inhibitor I2PP2A is essential for sister chromatid segregation in oocyte meiosis II. Curr Biol 2013; 23:485-90; PMID:23434280; https://doi.org/10.1016/j.cub.2013.02.004
   PubMed Web of Science ®Google Scholar
• Wassmann K. Sister chromatid segregation in meiosis II: deprotection through phosphorylation. Cell Cycle 2013; 12:1352-9; PMID:23574717; https://doi.org/10.4161/cc.24600
   PubMed Web of Science ®Google Scholar
• Higgins JM, Herbert M. Nucleosome assembly proteins get SET to defeat the guardian of chromosome cohesion. PLoS Genet 2013; 9:e1003829; PMID:24086159; https://doi.org/10.1371/journal.pgen.1003829
   PubMed Web of Science ®Google Scholar
• Arguello-Miranda O, Zagoriy I, Mengoli V, Rojas J, Jonak K, Oz T, Graf P, Zachariae W. Casein Kinase 1 Coordinates Cohesin Cleavage, Gametogenesis, and Exit from M Phase in Meiosis II. Dev Cell 2017; 40:37-52; PMID:28017619; https://doi.org/10.1016/j.devcel.2016.11.021
   PubMed Web of Science ®Google Scholar
• Matos J, Lipp JJ, Bogdanova A, Guillot S, Okaz E, Junqueira M, Shevchenko A, Zachariae W. Dbf4-dependent CDC7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 2008; 135:662-78; PMID:19013276; https://doi.org/10.1016/j.cell.2008.10.026
   PubMed Web of Science ®Google Scholar
• Liu X, Winey M. The MPS1 family of protein kinases. Annu Rev Biochem 2012; 81:561-85; PMID:22482908; https://doi.org/10.1146/annurev-biochem-061611-090435
   PubMed Web of Science ®Google Scholar
• Park YJ, Luger K. The structure of nucleosome assembly protein 1. Proc Natl Acad Sci U S A 2006; 103:1248-53; PMID:16432217; https://doi.org/10.1073/pnas.0508002103
   PubMed Web of Science ®Google Scholar
• Tang Y, Meeth K, Jiang E, Luo C, Marmorstein R. Structure of Vps75 and implications for histone chaperone function. Proc Natl Acad Sci U S A 2008; 105:12206-11; PMID:18723682; https://doi.org/10.1073/pnas.0802393105
   PubMed Web of Science ®Google Scholar
• Indjeian VB, Stern BM, Murray AW. The centromeric protein Sgo1 is required to sense lack of tension on mitotic chromosomes. Science 2005; 307:130-3; PMID:15637284; https://doi.org/10.1126/science.1101366
   PubMed Web of Science ®Google Scholar
• Maure JF, Kitamura E, Tanaka TU. Mps1 kinase promotes sister-kinetochore bi-orientation by a tension-dependent mechanism. Curr Biol 2007; 17:2175-82; PMID:18060784; https://doi.org/10.1016/j.cub.2007.11.032
   PubMed Web of Science ®Google Scholar
• Meyer RE, Kim S, Obeso D, Straight PD, Winey M, Dawson DS. Mps1 and Ipl1/Aurora B act sequentially to correctly orient chromosomes on the meiotic spindle of budding yeast. Science 2013; 339:1071-4; PMID:23371552; https://doi.org/10.1126/science.1232518
   PubMed Web of Science ®Google Scholar
• Hardwick KG, Weiss E, Luca FC, Winey M, Murray AW. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 1996; 273:953-6; PMID:8688079; https://doi.org/10.1126/science.273.5277.953
   PubMed Web of Science ®Google Scholar
• Palframan WJ, Meehl JB, Jaspersen SL, Winey M, Murray AW. Anaphase inactivation of the spindle checkpoint. Science 2006; 313:680-4; PMID:16825537; https://doi.org/10.1126/science.1127205
   PubMed Web of Science ®Google Scholar
• Okaz E, Arguello-Miranda O, Bogdanova A, Vinod PK, Lipp JJ, Markova Z, Zagoriy I, Novak B, Zachariae W. Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/CAma1. Cell 2012; 151:603-18; PMID:PMID:23101628; https://doi.org/10.1016/j.cell.2012.08.044
   PubMed Web of Science ®Google Scholar
• Kiburz BM, Reynolds DB, Megee PC, Marston AL, Lee BH, Lee TI, Levine SS, Young RA, Amon A. The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I. Genes Dev 2005; 19:3017-30; PMID:16357219; https://doi.org/10.1101/gad.1373005
   PubMed Web of Science ®Google Scholar
• Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, et al. Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 2010; 20:1511-21; PMID:20817533; https://doi.org/10.1016/j.cub.2010.08.023
   PubMed Web of Science ®Google Scholar
• Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 2010; 20:1522-8; PMID:20817534; https://doi.org/10.1016/j.cub.2010.06.069
   PubMed Web of Science ®Google Scholar
• Yun Y, Lane SI, Jones KT. Premature dyad separation in meiosis II is the major segregation error with maternal age in mouse oocytes. Development 2014; 141:199-208; PMID:24346700; https://doi.org/10.1242/dev.100206
   PubMed Web of Science ®Google Scholar
• Nabti I, Reis A, Levasseur M, Stemmann O, Jones KT. Securin and not CDK1/cyclin B1 regulates sister chromatid disjunction during meiosis II in mouse eggs. Dev Biol 2008; 321:379-86; PMID:18639540; https://doi.org/10.1016/j.ydbio.2008.06.036
   PubMed Web of Science ®Google Scholar
• Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW. Dual inhibition of sister chromatid separation at metaphase. Cell 2001; 107:715-26; PMID:11747808; https://doi.org/10.1016/S0092-8674(01)00603-1
   PubMed Web of Science ®Google Scholar
• Cui Y, Cheng X, Zhang C, Zhang Y, Li S, Wang C, Guadagno TM. Degradation of the human mitotic checkpoint kinase Mps1 is cell cycle-regulated by APC-cCdc20 and APC-cCdh1 ubiquitin ligases. J Biol Chem 2010; 285:32988-98; PMID:20729194; https://doi.org/10.1074/jbc.M110.140905
   PubMed Web of Science ®Google Scholar
• Tachikawa H, Bloecher A, Tatchell K, Neiman AM. A Gip1p-Glc7p phosphatase complex regulates septin organization and spore wall formation. J Cell Biol 2001; 155:797-808; PMID:11724821; https://doi.org/10.1083/jcb.200107008
   PubMed Web of Science ®Google Scholar