Cdc14 phosphatase directs centrosome re-duplication at the meiosis I to meiosis II transition in budding yeast [version 2; peer review: 4 approved]

Background : Gametes are generated through a specialized cell division called meiosis, in which ploidy is reduced by half because two consecutive rounds of chromosome segregation, meiosis I and meiosis II, occur without intervening DNA replication. This contrasts with the mitotic cell cycle where DNA replication and chromosome segregation alternate to maintain the same ploidy. At the end of mitosis, cyclin-dependent kinases (CDKs) are inactivated. This low CDK state in late mitosis/G1 allows for critical preparatory events for DNA replication and centrosome/spindle pole body (SPB) duplication. However, their execution is inhibited until S phase, where further preparatory events are also prevented. This “licensing” ensures that both the chromosomes and the centrosomes/SPBs replicate exactly once per cell cycle, thereby maintaining constant ploidy. Crucially, between meiosis I and meiosis II, centrosomes/SPBs must be re-licensed, but DNA re-replication must be avoided. In budding yeast, the Cdc14 protein phosphatase triggers CDK down regulation to promote exit from mitosis. Cdc14 also regulates the meiosis I to meiosis II transition, though its mode of action has remained unclear. Methods : Fluorescence and electron microscopy was combined with proteomics to probe SPB duplication in cells with inactive or hyperactive Cdc14. Results : We demonstrate

[1]  Sammie Bae,et al.  Graphs , 2020, Algorithms.

[2]  J. Rappsilber,et al.  Cdc14 phosphatase directs centrosome re-duplication at the meiosis I to meiosis II transition in budding yeast , 2017, Wellcome open research.

[3]  V. Sourjik,et al.  A FRET-based study reveals site-specific regulation of spindle position checkpoint proteins at yeast centrosomes , 2016, eLife.

[4]  G. Roeder,et al.  Cdc14 Early Anaphase Release, FEAR, Is Limited to the Nucleus and Dispensable for Efficient Mitotic Exit , 2015, PloS one.

[5]  J. Boulanger,et al.  Cell cycle control of spindle pole body duplication and splitting by Sfi1 and Cdc31 in fission yeast , 2015, Journal of Cell Science.

[6]  A. Marston,et al.  From equator to pole: splitting chromosomes in mitosis and meiosis , 2015, Genes & development.

[7]  Kwaku N. Opoku,et al.  Sister kinetochores are mechanically fused during meiosis I in yeast , 2014, Science.

[8]  E. Schiebel,et al.  Molecular Mechanisms that Restrict Yeast Centrosome Duplication to One Event per Cell Cycle , 2014, Current Biology.

[9]  B. Novák,et al.  CDK-Dependent Nuclear Localization of B-Cyclin Clb1 Promotes FEAR Activation during Meiosis I in Budding Yeast , 2013, PloS one.

[10]  A. Neiman,et al.  Sporulation in the Budding Yeast Saccharomyces cerevisiae , 2011, Genetics.

[11]  J. Millar,et al.  Meiotic nuclear divisions in budding yeast require PP2ACdc55-mediated antagonism of Net1 phosphorylation by Cdk , 2011, The Journal of cell biology.

[12]  J. Nickels,et al.  PP2ACdc55 is required for multiple events during meiosis I , 2011, Cell cycle.

[13]  L. Drury,et al.  Factors Affecting the Diversity of DNA Replication Licensing Control in Eukaryotes , 2009, Current Biology.

[14]  A. Amon,et al.  Cell polarity determinants establish asymmetry in MEN signaling. , 2009, Developmental cell.

[15]  A. Shevchenko,et al.  Dbf4-Dependent Cdc7 Kinase Links DNA Replication to the Segregation of Homologous Chromosomes in Meiosis I , 2008, Cell.

[16]  H. Maekawa,et al.  The yeast centrosome translates the positional information of the anaphase spindle into a cell cycle signal , 2007, The Journal of cell biology.

[17]  W. Huh,et al.  Bimolecular fluorescence complementation analysis system for in vivo detection of protein–protein interaction in Saccharomyces cerevisiae , 2007, Yeast.

[18]  A. Neiman,et al.  Cdc15 Is Required for Spore Morphogenesis Independently of Cdc14 in Saccharomyces cerevisiae , 2007, Genetics.

[19]  B. Chait,et al.  The nuclear pore complex–associated protein, Mlp2p, binds to the yeast spindle pole body and promotes its efficient assembly , 2005, The Journal of cell biology.

[20]  J. Julian Blow,et al.  Preventing re-replication of chromosomal DNA , 2005, Nature Reviews Molecular Cell Biology.

[21]  Masayuki Yamamoto,et al.  Fission yeast Mes1p ensures the onset of meiosis II by blocking degradation of cyclin Cdc13p , 2005, Nature.

[22]  Angelika Amon,et al.  Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. , 2004, Annual review of genetics.

[23]  J. Kilmartin.  Sfi1p has conserved centrin-binding sites and an essential function in budding yeast spindle pole body duplication , 2003, The Journal of cell biology.

[24]  Angelika Amon,et al.  The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation. , 2003, Developmental cell.

[25]  A. Amon,et al.  Role of Polo-like Kinase CDC5 in Programming Meiosis I Chromosome Segregation , 2003, Science.

[26]  S. Yoshida,et al.  Mitotic Exit Network Controls the Localization of Cdc14 to the Spindle Pole Body in Saccharomyces cerevisiae , 2002, Current Biology.

[27]  J. Grindlay,et al.  Regulation of the Bfa1p–Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p , 2002, The Journal of cell biology.

[28]  Angelika Amon,et al.  Separase, Polo Kinase, the Kinetochore Protein Slk19, and Spo12 Function in a Network that Controls Cdc14 Localization during Early Anaphase , 2002, Cell.

[29]  E. Salmon,et al.  Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. , 2001, Molecular biology of the cell.

[30]  K. Nasmyth,et al.  Disjunction of Homologous Chromosomes in Meiosis I Depends on Proteolytic Cleavage of the Meiotic Cohesin Rec8 by Separin , 2000, Cell.

[31]  T. Kishimoto,et al.  Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M–M transition in Xenopus oocyte extracts , 2000, The EMBO journal.

[32]  Peter K. Sorger,et al.  Transient Sister Chromatid Separation and Elastic Deformation of Chromosomes during Mitosis in Budding Yeast , 2000, Cell.

[33]  Angelika Amon,et al.  Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus , 1999, Nature.

[34]  Anna Shevchenko,et al.  Exit from Mitosis Is Triggered by Tem1-Dependent Release of the Protein Phosphatase Cdc14 from Nucleolar RENT Complex , 1999, Cell.

[35]  M. Tyers,et al.  The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. , 1998, Molecular cell.

[36]  D O Morgan,et al.  A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. , 1998, Molecular biology of the cell.

[37]  P. Philippsen,et al.  Additional modules for versatile and economical PCR‐based gene deletion and modification in Saccharomyces cerevisiae , 1998, Yeast.

[38]  E. Schiebel,et al.  The Cdc31p-binding protein Kar1p is a component of the half bridge of the yeast spindle pole body , 1995, The Journal of cell biology.

[39]  M. Winey,et al.  Genetic interactions between CDC31 and KAR1, two genes required for duplication of the microtubule organizing center in Saccharomyces cerevisiae. , 1994, Genetics.

[40]  E. Schiebel,et al.  The calcium-binding protein cell division cycle 31 of Saccharomyces cerevisiae is a component of the half bridge of the spindle pole body , 1993, The Journal of cell biology.

[41]  G. Simchen,et al.  Mixed segregation of chromosomes during single-division meiosis of Saccharomyces cerevisiae. , 1990, Genetics.

[42]  M. Mann,et al.  Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips , 2007, Nature Protocols.

[43]  S. Reed,et al.  Multi-step control of spindle pole body duplication by cyclin-dependent kinase , 2000, Nature Cell Biology.

[44]  B. Byers,et al.  Duplication of spindle plaques and integration of the yeast cell cycle. , 1974, Cold Spring Harbor symposia on quantitative biology.