Cdc14 phosphatase: warning, no delay allowed for chromosome segregation!

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• 作者：Félix Machín ; Oliver Quevedo ; Cristina Ramos-Pérez ; Jonay García-Luis
• 关键词：Cdc14 ; Saccharomyces cerevisiae ; rDNA ; Anaphase bridges ; Gross chromosomal rearrangements ; Aneuploidy
• 刊名：Current Genetics
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：62
• 期：1
• 页码：7-13
• 全文大小：534 KB
• 参考文献：Aguilera A, Gaillard H (2014) Transcription and recombination: when RNA Meets DNA. Cold Spring Harb Perspect Biol. doi:10.​1101/​cshperspect.​a016543 PubMed
  Bermejo R, Lai MS, Foiani M (2012) Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription. Mol Cell 45:710–718. doi:10.​1016/​j.​molcel.​2012.​03.​001 CrossRef PubMed
  Blanco MG, Matos J, West SC (2014) Dual control of Yen1 nuclease activity and cellular localization by Cdk and Cdc14 prevents genome instability. Mol Cell 54:94–106. doi:10.​1016/​j.​molcel.​2014.​02.​011 PubMedCentral CrossRef PubMed
  Clemente-Blanco A, Mayán-Santos M, Schneider DA et al (2009) Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 458:219–222. doi:10.​1038/​nature07652 PubMedCentral CrossRef PubMed
  Clemente-Blanco A, Sen N, Mayan-Santos M et al (2011) Cdc14 phosphatase promotes segregation of telomeres through repression of RNA polymerase II transcription. Nat Cell Biol 13:1450–1456. doi:10.​1038/​ncb2365 PubMedCentral CrossRef PubMed
  D’Ambrosio C, Kelly G, Shirahige K, Uhlmann F (2008) Condensin-dependent rDNA decatenation introduces a temporal pattern to chromosome segregation. Curr Biol 18:1084–1089. doi:10.​1016/​j.​cub.​2008.​06.​058 CrossRef PubMed
  D’Amours D, Stegmeier F, Amon A (2004) Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117:455–469CrossRef PubMed
  De Wulf P, Montani F, Visintin R (2009) Protein phosphatases take the mitotic stage. Curr Opin Cell Biol 21:806–815. doi:10.​1016/​j.​ceb.​2009.​08.​003 CrossRef PubMed
  Dulev S, de Renty C, Mehta R et al (2009) Essential global role of CDC14 in DNA synthesis revealed by chromosome underreplication unrecognized by checkpoints in cdc14 mutants. Proc Natl Acad Sci USA 106:14466–14471. doi:10.​1073/​pnas.​0900190106 PubMedCentral CrossRef PubMed
  Eissler CL, Mazón G, Powers BL et al (2014) The Cdk/Cdc14 module controls activation of the Yen1 Holliday junction resolvase to promote genome stability. Mol Cell 54:80–93. doi:10.​1016/​j.​molcel.​2014.​02.​012 PubMedCentral CrossRef PubMed
  Freeman L, Aragon-Alcaide L, Strunnikov A (2000) The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol 149:811–824PubMedCentral CrossRef PubMed
  García-Luis J, Machín F (2014) Mus81-Mms4 and Yen1 resolve a novel anaphase bridge formed by noncanonical Holliday junctions. Nat Commun 5:5652. doi:10.​1038/​ncomms6652 CrossRef PubMed
  García-Luis J, Clemente-Blanco A, Aragón L, Machín F (2014) Cdc14 targets the Holliday junction resolvase Yen1 to the nucleus in early anaphase. Cell Cycle 13:1392–1399. doi:10.​4161/​cc.​28370 PubMedCentral CrossRef PubMed
  Geil C, Schwab M, Seufert W (2008) A nucleolus-localized activator of Cdc14 phosphatase supports rDNA segregation in yeast mitosis. Curr Biol 18:1001–1005. doi:10.​1016/​j.​cub.​2008.​06.​025 CrossRef PubMed
  Germann SM, Schramke V, Pedersen RT et al (2014) TopBP1/Dpb11 binds DNA anaphase bridges to prevent genome instability. J Cell Biol 204:45–59. doi:10.​1083/​jcb.​201305157 PubMedCentral CrossRef PubMed
  Granot D, Snyder M (1991) Segregation of the nucleolus during mitosis in budding and fission yeast. Cell Motil Cytoskeleton 20:47–54. doi:10.​1002/​cm.​970200106 CrossRef PubMed
  Guacci V, Hogan E, Koshland D (1994) Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol 125:517–530CrossRef PubMed
  Harrison BD, Hoang ML, Bloom K (2009) Persistent mechanical linkage between sister chromatids throughout anaphase. Chromosoma 118:633–645. doi:10.​1007/​s00412-009-0224-6 PubMedCentral CrossRef PubMed
  Hirano T (2012) Condensins: universal organizers of chromosomes with diverse functions. Genes Dev 26:1659–1678. doi:10.​1101/​gad.​194746.​112 PubMedCentral CrossRef PubMed
  Holm C, Goto T, Wang JC, Botstein D (1985) DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41:553–563CrossRef PubMed
  Jin F, Liu H, Liang F et al (2008) Temporal control of the dephosphorylation of Cdk substrates by mitotic exit pathways in budding yeast. Proc Natl Acad Sci USA 105:16177–16182. doi:10.​1073/​pnas.​0808719105 PubMedCentral CrossRef PubMed
  Kaiser BK, Zimmerman ZA, Charbonneau H, Jackson PK (2002) Disruption of centrosome structure, chromosome segregation, and cytokinesis by misexpression of human Cdc14A phosphatase. Mol Biol Cell 13:2289–2300. doi:10.​1091/​mbc.​01-11-0535 PubMedCentral CrossRef PubMed
  Kobayashi T, Horiuchi T (1996) A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1:465–474CrossRef PubMed
  Lavoie BD, Hogan E, Koshland D (2004) In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev 18:76–87. doi:10.​1101/​gad.​1150404 PubMedCentral CrossRef PubMed
  Machín F, Torres-Rosell J, Jarmuz A, Aragón L (2005) Spindle-independent condensation-mediated segregation of yeast ribosomal DNA in late anaphase. J Cell Biol 168:209–219. doi:10.​1083/​jcb.​200408087 PubMedCentral CrossRef PubMed
  Machín F, Torres-Rosell J, De Piccoli G et al (2006) Transcription of ribosomal genes can cause nondisjunction. J Cell Biol 173:893–903. doi:10.​1083/​jcb.​200511129 PubMedCentral CrossRef PubMed
  Mailand N, Lukas C, Kaiser BK et al (2002) Deregulated human Cdc14A phosphatase disrupts centrosome separation and chromosome segregation. Nat Cell Biol 4:317–322. doi:10.​1038/​ncb777 CrossRef PubMed
  McClintock B (1939) The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc Natl Acad Sci USA 25:405–416PubMedCentral CrossRef PubMed
  Meitinger F, Palani S, Pereira G (2012) The power of MEN in cytokinesis. Cell Cycle 11:219–228. doi:10.​4161/​cc.​11.​2.​18857 CrossRef PubMed
  Mocciaro A, Schiebel E (2010) Cdc14: a highly conserved family of phosphatases with non-conserved functions? J Cell Sci 123:2867–2876. doi:10.​1242/​jcs.​074815 CrossRef PubMed
  Petes TD (1979) Meiotic mapping of yeast ribosomal deoxyribonucleic acid on chromosome XII. J Bacteriol 138:185–192PubMedCentral PubMed
  Quevedo O, García-Luis J, Matos-Perdomo E et al (2012) Nondisjunction of a single chromosome leads to breakage and activation of DNA damage checkpoint in g2. PLoS Genet 8:e1002509. doi:10.​1371/​journal.​pgen.​1002509 PubMedCentral CrossRef PubMed
  Quevedo O, Ramos-Perez C, Petes TD, Machin F (2015) The transient inactivation of the master cell cycle phosphatase Cdc14 causes genomic instability in diploid cells of Saccharomyces cerevisiae. Genetics. doi:10.​1534/​genetics.​115.​177626 PubMed
  Renshaw MJ, Ward JJ, Kanemaki M et al (2010) Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev Cell 19:232–244. doi:10.​1016/​j.​devcel.​2010.​07.​013 PubMedCentral CrossRef PubMed
  Roccuzzo M, Visintin C, Tili F, Visintin R (2015) FEAR-mediated activation of Cdc14 is the limiting step for spindle elongation and anaphase progression. Nat Cell Biol 17:251–261. doi:10.​1038/​ncb3105 CrossRef PubMed
  Ross KE, Cohen-Fix O (2004) A role for the FEAR pathway in nuclear positioning during anaphase. Dev Cell 6:729–735CrossRef PubMed
  Stegmeier F, Amon A (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38:203–232. doi:10.​1146/​annurev.​genet.​38.​072902.​093051 CrossRef PubMed
  Stegmeier F, Visintin R, Amon A (2002) Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase. Cell 108:207–220CrossRef PubMed
  Sullivan M, Higuchi T, Katis VL, Uhlmann F (2004) Cdc14 phosphatase induces rDNA condensation and resolves cohesin-independent cohesion during budding yeast anaphase. Cell 117:471–482CrossRef PubMed
  Tang Z, Shu H, Qi W et al (2006) PP2A Is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev Cell 10:575–585. doi:10.​1016/​j.​devcel.​2006.​03.​010 CrossRef PubMed
  Titos I, Ivanova T, Mendoza M (2014) Chromosome length and perinuclear attachment constrain resolution of DNA intertwines. J Cell Biol 206:719–733. doi:10.​1083/​jcb.​201404039 PubMedCentral CrossRef PubMed
  Tomson BN, D’Amours D, Adamson BS et al (2006) Ribosomal DNA transcription-dependent processes interfere with chromosome segregation. Mol Cell Biol 26:6239–6247. doi:10.​1128/​MCB.​00693-06 PubMedCentral CrossRef PubMed
  Torres-Rosell J, Machín F, Jarmuz A, Aragón L (2004) Nucleolar segregation lags behind the rest of the genome and requires Cdc14p activation by the FEAR network. Cell Cycle 3:496–502CrossRef PubMed
  Torres-Rosell J, Machín F, Aragón L (2005) Cdc14 and the temporal coordination between mitotic exit and chromosome segregation. Cell Cycle 4:109–112CrossRef PubMed
  Torres-Rosell J, De Piccoli G, Cordon-Preciado V et al (2007) Anaphase onset before complete DNA replication with intact checkpoint responses. Science 315:1411–1415. doi:10.​1126/​science.​1134025 CrossRef PubMed
  Uhlmann F, Bouchoux C, Lopez-Aviles S (2011) A quantitative model for cyclin-dependent kinase control of the cell cycle: revisited. Philos Trans R Soc B Biol Sci 366:3572–3583. doi:10.​1098/​rstb.​2011.​0082 CrossRef
  Varela E, Shimada K, Laroche T et al (2009) Lte1, Cdc14 and MEN-controlled Cdk inactivation in yeast coordinate rDNA decompaction with late telophase progression. EMBO J 28:1562–1575. doi:10.​1038/​emboj.​2009.​111 PubMedCentral CrossRef PubMed
  Wang B-D, Yong-Gonzalez V, Strunnikov AV (2004) Cdc14p/FEAR pathway controls segregation of nucleolus in S. cerevisiae by facilitating condensin targeting to rDNA chromatin in anaphase. Cell Cycle 3:960–967PubMedCentral PubMed
  Weiss EL (2012) Mitotic exit and separation of mother and daughter cells. Genetics 192:1165–1202. doi:10.​1534/​genetics.​112.​145516 PubMedCentral CrossRef PubMed
  Wurzenberger C, Gerlich DW (2011) Phosphatases: providing safe passage through mitotic exit. Nat Rev Mol Cell Biol 12:469–482. doi:10.​1038/​nrm3149 CrossRef PubMed
  
• 作者单位：Félix Machín (1)
  Oliver Quevedo (1) (2)
  Cristina Ramos-Pérez (1)
  Jonay García-Luis (1) (3)
  
  1. Unidad de Investigación, Hospital Universitario Nuestra Señora de la Candelaria, Ctra del Rosario 145, 38010, Santa Cruz de Tenerife, Spain
  2. Center for Chromosome Stability and Department of Biology, University of Copenhagen, 2200, Copenhagen, Denmark
  3. Cell Cycle Group, MRC Clinical Sciences Centre, Imperial College London, Du Cane Road, London, W12 0NN, UK
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Microbial Genetics and Genomics
  Microbiology
  Biochemistry
  Cell Biology
  Plant Sciences
  Proteomics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0983

文摘

Cycling events in nature start and end to restart again and again. In the cell cycle, whose purpose is to become two where there was only one, cyclin-dependent kinases (CDKs) are the beginning and, therefore, phosphatases must play a role in the ending. Since CDKs are drivers of the cell cycle and cancer cells uncontrollably divide, much attention has been put into knocking down CDK activity. However, much less is known on the consequences of interfering with the phosphatases that put an end to the cell cycle. We have addressed in recent years the consequences of transiently inactivating the only master cell cycle phosphatase in the model yeast Saccharomyces cerevisiae, Cdc14. Transient inactivation is expected to better mimic the pharmacological action of drugs. Interestingly, we have found that yeast cells tolerate badly a relatively brief inactivation of Cdc14 when cells are already committed into anaphase, the first cell cycle stage where this phosphatase plays important roles. First, we noticed that the segregation of distal regions in the chromosome arm that carries the ribosomal DNA array was irreversibly impaired, leading to an anaphase bridge (AB). Next, we found that this AB could eventually be severed by cytokinesis and led to two different types of genetically compromised daughter cells. All these previous studies were done in haploid cells. We have now recently expanded this analysis to diploid cells and used the advantage of making hybrid diploids to study chromosome rearrangements and changes in the ploidy of the surviving progeny. We have found that the consequences for the genome integrity were far more dramatic than originally envisioned. Keywords Cdc14 Saccharomyces cerevisiae rDNA Anaphase bridges Gross chromosomal rearrangements Aneuploidy