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An E2 enzyme Ubc11 is required for ubiquitination of Slp1/Cdc20 and spindle checkpoint silencing in fission yeast

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Pages 961-971 | Published online: 26 Feb 2013

References

  • Peters JM. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 2002; 9:931 - 43; http://dx.doi.org/10.1016/S1097-2765(02)00540-3; PMID: 12049731
  • Pines J. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol 2006; 16:55 - 63; http://dx.doi.org/10.1016/j.tcb.2005.11.006; PMID: 16337124
  • Sullivan M, Morgan DO. Finishing mitosis, one step at a time. Nat Rev Mol Cell Biol 2007; 8:894 - 903; http://dx.doi.org/10.1038/nrm2276; PMID: 17912263
  • Schwab M, Lutum AS, Seufert W. Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 1997; 90:683 - 93; http://dx.doi.org/10.1016/S0092-8674(00)80529-2; PMID: 9288748
  • Visintin R, Prinz S, Amon A. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 1997; 278:460 - 3; http://dx.doi.org/10.1126/science.278.5337.460; PMID: 9334304
  • Fang G, Yu H, Kirschner MW. Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1. Mol Cell 1998; 2:163 - 71; http://dx.doi.org/10.1016/S1097-2765(00)80126-4; PMID: 9734353
  • Kramer ER, Gieffers C, Hölzl G, Hengstschläger M, Peters JM. Activation of the human anaphase-promoting complex by proteins of the CDC20/Fizzy family. Curr Biol 1998; 8:1207 - 10; http://dx.doi.org/10.1016/S0960-9822(07)00510-6; PMID: 9811605
  • Pfleger CM, Kirschner MW. The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev 2000; 14:655 - 65; PMID: 10733526
  • Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 2007; 8:379 - 93; http://dx.doi.org/10.1038/nrm2163; PMID: 17426725
  • Rieder CL, Schultz A, Cole R, Sluder G. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J Cell Biol 1994; 127:1301 - 10; http://dx.doi.org/10.1083/jcb.127.5.1301; PMID: 7962091
  • Rieder CL, Cole RW, Khodjakov A, Sluder G. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 1995; 130:941 - 8; http://dx.doi.org/10.1083/jcb.130.4.941; PMID: 7642709
  • Hardwick KG, Johnston RC, Smith DL, Murray AW. MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J Cell Biol 2000; 148:871 - 82; http://dx.doi.org/10.1083/jcb.148.5.871; PMID: 10704439
  • Sudakin V, Chan GK, Yen TJ. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 2001; 154:925 - 36; http://dx.doi.org/10.1083/jcb.200102093; PMID: 11535616
  • Burton JL, Solomon MJ. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev 2007; 21:655 - 67; http://dx.doi.org/10.1101/gad.1511107; PMID: 17369399
  • Herzog F, Primorac I, Dube P, Lenart P, Sander B, Mechtler K, et al. Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science 2009; 323:1477 - 81; http://dx.doi.org/10.1126/science.1163300; PMID: 19286556
  • Chao WC, Kulkarni K, Zhang Z, Kong EH, Barford D. Structure of the mitotic checkpoint complex. Nature 2012; 484:208 - 13; http://dx.doi.org/10.1038/nature10896; PMID: 22437499
  • Reddy SK, Rape M, Margansky WA, Kirschner MW. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 2007; 446:921 - 5; http://dx.doi.org/10.1038/nature05734; PMID: 17443186
  • Nilsson J, Yekezare M, Minshull J, Pines J. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat Cell Biol 2008; 10:1411 - 20; http://dx.doi.org/10.1038/ncb1799; PMID: 18997788
  • Jia L, Li B, Warrington RT, Hao X, Wang S, Yu H. Defining pathways of spindle checkpoint silencing: functional redundancy between Cdc20 ubiquitination and p31(comet). Mol Biol Cell 2011; 22:4227 - 35; http://dx.doi.org/10.1091/mbc.E11-05-0389; PMID: 21937719
  • Mansfeld J, Collin P, Collins MO, Choudhary JS, Pines J. APC15 drives the turnover of MCC-CDC20 to make the spindle assembly checkpoint responsive to kinetochore attachment. Nat Cell Biol 2011; 13:1234 - 43; http://dx.doi.org/10.1038/ncb2347; PMID: 21926987
  • Habu T, Kim SH, Weinstein J, Matsumoto T. Identification of a MAD2-binding protein, CMT2, and its role in mitosis. EMBO J 2002; 21:6419 - 28; http://dx.doi.org/10.1093/emboj/cdf659; PMID: 12456649
  • Dobles M, Liberal V, Scott ML, Benezra R, Sorger PK. Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 2000; 101:635 - 45; http://dx.doi.org/10.1016/S0092-8674(00)80875-2; PMID: 10892650
  • Hoyt MA, Totis L, Roberts BTS. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 1991; 66:507 - 17; http://dx.doi.org/10.1016/0092-8674(81)90014-3; PMID: 1651171
  • Roberts BT, Farr KA, Hoyt MA. The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase. Mol Cell Biol 1994; 14:8282 - 91; PMID: 7969164
  • Hardwick KG, Murray AW. Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J Cell Biol 1995; 131:709 - 20; http://dx.doi.org/10.1083/jcb.131.3.709; PMID: 7593191
  • He X, Patterson TE, Sazer S. The Schizosaccharomyces pombe spindle checkpoint protein mad2p blocks anaphase and genetically interacts with the anaphase-promoting complex. Proc Natl Acad Sci USA 1997; 94:7965 - 70; http://dx.doi.org/10.1073/pnas.94.15.7965; PMID: 9223296
  • Bernard P, Hardwick K, Javerzat JP. Fission yeast bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J Cell Biol 1998; 143:1775 - 87; http://dx.doi.org/10.1083/jcb.143.7.1775; PMID: 9864354
  • Chen RH, Brady DM, Smith D, Murray AW, Hardwick KG. The spindle checkpoint of budding yeast depends on a tight complex between the Mad1 and Mad2 proteins. Mol Biol Cell 1999; 10:2607 - 18; PMID: 10436016
  • Millband DN, Hardwick KG. Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner. Mol Cell Biol 2002; 22:2728 - 42; http://dx.doi.org/10.1128/MCB.22.8.2728-2742.2002; PMID: 11909965
  • Ikui AE, Furuya K, Yanagida M, Matsumoto T. Control of localization of a spindle checkpoint protein, Mad2, in fission yeast. J Cell Sci 2002; 115:1603 - 10; PMID: 11950879
  • Tanaka K, Yonekawa T, Kawasaki Y, Kai M, Furuya K, Iwasaki M, et al. Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol Cell Biol 2000; 20:3459 - 69; http://dx.doi.org/10.1128/MCB.20.10.3459-3469.2000; PMID: 10779336
  • Nakamura T, Nakamura-Kubo M, Hirata A, Shimoda C. The Schizosaccharomyces pombe spo3+ gene is required for assembly of the forespore membrane and genetically interacts with psy1(+)-encoding syntaxin-like protein. Mol Biol Cell 2001; 12:3955 - 72; PMID: 11739793
  • Osaka F, Seino H, Seno T, Yamao F. A ubiquitin-conjugating enzyme in fission yeast that is essential for the onset of anaphase in mitosis. Mol Cell Biol 1997; 17:3388 - 97; PMID: 9154838
  • Kim SH, Lin DP, Matsumoto S, Kitazono A, Matsumoto T. Fission yeast Slp1: an effector of the Mad2-dependent spindle checkpoint. Science 1998; 279:1045 - 7; http://dx.doi.org/10.1126/science.279.5353.1045; PMID: 9461438
  • Ye Y, Rape M. Building ubiquitin chains: E2 enzymes at work. Nat Rev Mol Cell Biol 2009; 10:755 - 64; http://dx.doi.org/10.1038/nrm2780; PMID: 19851334
  • Yanagida M. Fission yeast cut mutations revisited: control of anaphase. Trends Cell Biol 1998; 8:144 - 9; http://dx.doi.org/10.1016/S0962-8924(98)01236-7; PMID: 9695827
  • Seino H, Kishi T, Nishitani H, Yamao F. Two ubiquitin-conjugating enzymes, UbcP1/Ubc4 and UbcP4/Ubc11, have distinct functions for ubiquitination of mitotic cyclin. Mol Cell Biol 2003; 23:3497 - 505; http://dx.doi.org/10.1128/MCB.23.10.3497-3505.2003; PMID: 12724408
  • Glotzer M, Murray AW, Kirschner MW. Cyclin is degraded by the ubiquitin pathway. Nature 1991; 349:132 - 8; http://dx.doi.org/10.1038/349132a0; PMID: 1846030
  • Yamano H, Gannon J, Hunt T. The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe. EMBO J 1996; 15:5268 - 79; PMID: 8895572
  • Funabiki H, Kumada K, Yanagida M. Fission yeast Cut1 and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes. EMBO J 1996; 15:6617 - 28; PMID: 8978688
  • Funabiki H, Yamano H, Nagao K, Tanaka H, Yasuda H, Hunt T, et al. Fission yeast Cut2 required for anaphase has two destruction boxes. EMBO J 1997; 16:5977 - 87; http://dx.doi.org/10.1093/emboj/16.19.5977; PMID: 9312055
  • Hiraoka Y, Toda T, Yanagida M. The NDA3 gene of fission yeast encodes beta-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 1984; 39:349 - 58; http://dx.doi.org/10.1016/0092-8674(84)90013-8; PMID: 6094012
  • Funabiki H, Yamano H, Kumada K, Nagao K, Hunt T, Yanagida M. Cut2 proteolysis required for sister-chromatid seperation in fission yeast. Nature 1996; 381:438 - 41; http://dx.doi.org/10.1038/381438a0; PMID: 8632802
  • Aoki K, Nakaseko Y, Kinoshita K, Goshima G, Yanagida M. CDC2 phosphorylation of the fission yeast dis1 ensures accurate chromosome segregation. Curr Biol 2006; 16:1627 - 35; http://dx.doi.org/10.1016/j.cub.2006.06.065; PMID: 16920624
  • Yamashita YM, Nakaseko Y, Samejima I, Kumada K, Yamada H, Michaelson D, et al. 20S cyclosome complex formation and proteolytic activity inhibited by the cAMP/PKA pathway. Nature 1996; 384:276 - 9; http://dx.doi.org/10.1038/384276a0; PMID: 8918880
  • Berry LD, Feoktistova A, Wright MD, Gould KL. The schizosaccharomyces pombe dim1(+) gene interacts with the anaphase-promoting complex or cyclosome (APC/C) component lid1(+) and is required for APC/C function. Mol Cell Biol 1999; 19:2535 - 46; PMID: 10082519
  • Yoon HJ, Feoktistova A, Wolfe BA, Jennings JL, Link AJ, Gould KL. Proteomics analysis identifies new components of the fission and budding yeast anaphase-promoting complexes. Curr Biol 2002; 12:2048 - 54; http://dx.doi.org/10.1016/S0960-9822(02)01331-3; PMID: 12477395
  • Takayama Y, Mamnun YM, Trickey M, Dhut S, Masuda F, Yamano H, et al. Hsk1- and SCF(Pof3)-dependent proteolysis of S. pombe Ams2 ensures histone homeostasis and centromere function. Dev Cell 2010; 18:385 - 96; http://dx.doi.org/10.1016/j.devcel.2009.12.024; PMID: 20230746
  • Gordon C, McGurk G, Wallace M, Hastie ND. A conditional lethal mutant in the fission yeast 26 S protease subunit mts3+ is defective in metaphase to anaphase transition. J Biol Chem 1996; 271:5704 - 11; http://dx.doi.org/10.1074/jbc.271.10.5704; PMID: 8621436
  • Hirano T, Funahashi S, Uemura T, Yanagida M. Isolation and characterization of Schizosaccharomyces pombe cutmutants that block nuclear division but not cytokinesis. EMBO J 1986; 5:2973 - 9; PMID: 16453724
  • Matsumoto T. A fission yeast homolog of CDC20/p55CDC/Fizzy is required for recovery from DNA damage and genetically interacts with p34cdc2. Mol Cell Biol 1997; 17:742 - 50; PMID: 9001228
  • Yamada HY, Matsumoto S, Matsumoto T. High dosage expression of a zinc finger protein, Grt1, suppresses a mutant of fission yeast slp1(+), a homolog of CDC20/p55CDC/Fizzy. J Cell Sci 2000; 113:3989 - 99; PMID: 11058086
  • Ohi MD, Feoktistova A, Ren L, Yip C, Cheng Y, Chen JS, et al. Structural organization of the anaphase-promoting complex bound to the mitotic activator Slp1. Mol Cell 2007; 28:871 - 85; http://dx.doi.org/10.1016/j.molcel.2007.10.003; PMID: 18082611
  • Pan J, Chen RH. Spindle checkpoint regulates Cdc20p stability in Saccharomyces cerevisiae. Genes Dev 2004; 18:1439 - 51; http://dx.doi.org/10.1101/gad.1184204; PMID: 15198982
  • Kirkpatrick DS, Hathaway NA, Hanna J, Elsasser S, Rush J, Finley D, et al. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat Cell Biol 2006; 8:700 - 10; http://dx.doi.org/10.1038/ncb1436; PMID: 16799550
  • Jin L, Williamson A, Banerjee S, Philipp I, Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008; 133:653 - 65; http://dx.doi.org/10.1016/j.cell.2008.04.012; PMID: 18485873
  • Matsumoto ML, Wickliffe KE, Dong KC, Yu C, Bosanac I, Bustos D, et al. K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol Cell 2010; 39:477 - 84; http://dx.doi.org/10.1016/j.molcel.2010.07.001; PMID: 20655260
  • Dimova NV, Hathaway NA, Lee BH, Kirkpatrick DS, Berkowitz ML, Gygi SP, et al. APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat Cell Biol 2012; 14:168 - 76; http://dx.doi.org/10.1038/ncb2425; PMID: 22286100
  • Summers MK, Pan B, Mukhyala K, Jackson PK. The unique N terminus of the UbcH10 E2 enzyme controls the threshold for APC activation and enhances checkpoint regulation of the APC. Mol Cell 2008; 31:544 - 56; http://dx.doi.org/10.1016/j.molcel.2008.07.014; PMID: 18722180
  • Foster SA, Morgan DO. The APC/C subunit Mnd2/Apc15 promotes Cdc20 autoubiquitination and spindle assembly checkpoint inactivation. Mol Cell 2012; 47:921 - 32; http://dx.doi.org/10.1016/j.molcel.2012.07.031; PMID: 22940250
  • Uzunova K, Dye BT, Schutz H, Ladurner R, Petzold G, Toyoda Y, et al. APC15 mediates CDC20 autoubiquitylation by APC/C(MCC) and disassembly of the mitotic checkpoint complex. Nat Struct Mol Biol 2012; 19:1116 - 23; http://dx.doi.org/10.1038/nsmb.2412; PMID: 23007861
  • Beach D, Rodgers L, Gould J. ran1+ controls the transition from mitotic division to meiosis in fission yeast. Curr Genet 1985; 10:297 - 311; http://dx.doi.org/10.1007/BF00365626; PMID: 3870979
  • Cottarel G. The Saccharomyces cerevisiae HIS3 and LYS2 genes complement the Schizosaccharomyces pombe his5-303 and lys1-131 mutations, respectively: new selectable markers and new multi-purpose multicopy shuttle vectors, pSP3 and pSP4. Curr Genet 1995; 28:380 - 3; http://dx.doi.org/10.1007/BF00326437; PMID: 8590485
  • Takayama Y, Sato H, Saitoh S, Ogiyama Y, Masuda F, Takahashi K. Biphasic incorporation of centromeric histone CENP-A in fission yeast. Mol Biol Cell 2008; 19:682 - 90; http://dx.doi.org/10.1091/mbc.E07-05-0504; PMID: 18077559
  • Okazaki K, Okazaki N, Kume K, Jinno S, Tanaka K, Okayama H. High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res 1990; 18:6485 - 9; http://dx.doi.org/10.1093/nar/18.22.6485; PMID: 2251111
  • Gietz D, St Jean A, Woods RA, Schiestl RH. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 1992; 20:1425; http://dx.doi.org/10.1093/nar/20.6.1425; PMID: 1561104
  • Jensen R, Sprague GF Jr., Herskowitz I. Regulation of yeast mating-type interconversion: feedback control of HO gene expression by the mating-type locus. Proc Natl Acad Sci USA 1983; 80:3035 - 9; http://dx.doi.org/10.1073/pnas.80.10.3035; PMID: 6344075
  • Ito D, Saito Y, Matsumoto T. Centromere-tethered Mps1 pombe homolog (Mph1) kinase is a sufficient marker for recruitment of the spindle checkpoint protein Bub1, but not Mad1. Proc Natl Acad Sci USA 2012; 109:209 - 14; http://dx.doi.org/10.1073/pnas.1114647109; PMID: 22184248
  • Matsumoto T, Beach D. Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase. Cell 1991; 66:347 - 60; http://dx.doi.org/10.1016/0092-8674(91)90624-8; PMID: 1855255
  • Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998; 14:953 - 61; http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U; PMID: 9717241
  • Matsuyama A, Shirai A, Yoshida M. A series of promoters for constitutive expression of heterologous genes in fission yeast. Yeast 2008; 25:371 - 6; http://dx.doi.org/10.1002/yea.1593; PMID: 18437702

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