The ribosomal DNA metaphase loop of Saccharomyces cerevisiae gets condensed upon heat stress in a Cdc14-independent TORC1-dependent manner

References

• Edgar RS, Lielausis I. Temperature-sensitive mutants of bacteriophage T4D: Their isolation and genetic characterization. Genetics. 1964;49:649–662. PMID:14156925
   PubMed Web of Science ®Google Scholar
• Basilico C. Temperature-sensitive mutations in animal cells. Adv Cancer Res. 1977;24:223–266. doi:10.1016/S0065-230X(08)61016-7. PMID:322459
   PubMedGoogle Scholar
• Hartwell LH. Macromolecule synthesis in temperature-sensitive mutants of yeast. J Bacteriol. 1967;93:1662–1670. PMID:5337848
   PubMed Web of Science ®Google Scholar
• Hartwell LH. Three additional genes required for deoxyribonucleic acid synthesis in Saccharomyces cerevisiae. J Bacteriol. 1973;115:966–974. PMID:4580573
   PubMed Web of Science ®Google Scholar
• Hartwell LH, Culotti J, Pringle JR, et al. Genetic control of the cell division cycle in yeast. Science. 1974;183:46–51. doi:10.1126/science.183.4120.46. PMID:4587263
   PubMed Web of Science ®Google Scholar
• Warner JR, Udem SA. Temperature sensitive mutations affecting ribosome synthesis in Saccharomyces cerevisiae. J Mol Biol. 1972;65:243–257. doi:10.1016/0022-2836(72)90280-X. PMID:4557193
   PubMed Web of Science ®Google Scholar
• Kschonsak M, Haering CH. Shaping mitotic chromosomes: From classical concepts to molecular mechanisms. Bioessays. 2015;37:755–766. doi:10.1002/bies.201500020. PMID:25988527
   PubMed Web of Science ®Google Scholar
• Hirano T. Condensin-Based Chromosome Organization from Bacteria to Vertebrates. Cell. 2016;164:847–857. doi:10.1016/j.cell.2016.01.033. PMID:26919425
   PubMed Web of Science ®Google Scholar
• Guacci V, Hogan E, Koshland D. Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol. 1994;125:517–530. doi:10.1083/jcb.125.3.517. PMID:8175878
   PubMed Web of Science ®Google Scholar
• Torres-Rosell J, Machín F, Jarmuz A, et al. Nucleolar segregation lags behind the rest of the genome and requires Cdc14p activation by the FEAR network. Cell Cycle. 2004;3:496–502. doi:10.4161/cc.3.4.802. PMID:15004526
   PubMed Web of Science ®Google Scholar
• Renshaw MJ, Ward JJ, Kanemaki M, et al. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev Cell. 2010;19:232–244. doi:10.1016/j.devcel.2010.07.013. PMID:20708586
   PubMed Web of Science ®Google Scholar
• Strunnikov AV, Larionov VL, Koshland D. SMC1: An essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol. 1993;123:1635–1648. doi:10.1083/jcb.123.6.1635. PMID:8276886
   PubMed Web of Science ®Google Scholar
• Strunnikov AV, Hogan E, Koshland D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev. 1995;9:587–599. doi:10.1101/gad.9.5.587. PMID:7698648
   PubMed Web of Science ®Google Scholar
• Holm C, Goto T, Wang JC, et al. DNA topoisomerase II is required at the time of mitosis in yeast. Cell 1985;41:553–563. doi:10.1016/S0092-8674(85)80028-3. PMID:2985283
   PubMed Web of Science ®Google Scholar
• Michaelis C, Ciosk R, Nasmyth K. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997;91:35–45. doi:10.1016/S0092-8674(01)80007-6. PMID:9335333
   PubMed Web of Science ®Google Scholar
• Uhlmann F, Lottspeich F, Nasmyth K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature. 1999;400:37–42. doi:10.1038/21831. PMID:10403247
   PubMed Web of Science ®Google Scholar
• Freeman L, Aragon-Alcaide L, Strunnikov A. The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol. 2000;149:811–824. doi:10.1083/jcb.149.4.811. PMID:10811823
   PubMed Web of Science ®Google Scholar
• Lavoie BD, Hogan E, Koshland D. In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J Cell Biol. 2002;156:805–815. doi:10.1083/jcb.200109056. PMID:11864994
   PubMed Web of Science ®Google Scholar
• Lavoie BD, Hogan E, Koshland D. In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev. 2004;18:76–87. doi:10.1101/gad.1150404. PMID:14701879
   PubMed Web of Science ®Google Scholar
• Alexandru G, Uhlmann F, Mechtler K, et al. Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell. 2001;105:459–472. doi:10.1016/S0092-8674(01)00362-2. PMID:11371343
   PubMed Web of Science ®Google Scholar
• D'Amours D, Stegmeier F, Amon A. Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell. 2004;117:455–469. doi:10.1016/S0092-8674(04)00413-1. PMID:15137939
   PubMed Web of Science ®Google Scholar
• Machín F, Torres-Rosell J, Jarmuz A, et al. Spindle-independent condensation-mediated segregation of yeast ribosomal DNA in late anaphase. J Cell Biol. 2005;168:209–219. doi:10.1083/jcb.200408087. PMID:15657393
   PubMed Web of Science ®Google Scholar
• Sullivan M, Higuchi T, Katis VL, et al. Cdc14 phosphatase induces rDNA condensation and resolves cohesin-independent cohesion during budding yeast anaphase. Cell 2004;117:471–482. doi:10.1016/S0092-8674(04)00415-5. PMID:15137940
   PubMed Web of Science ®Google Scholar
• Yoshida S, Toh-e A. Budding yeast Cdc5 phosphorylates Net1 and assists Cdc14 release from the nucleolus. Biochem Biophys Res Commun. 2002;294:687–691. doi:10.1016/S0006-291X(02)00544-2. PMID:12056824
   PubMed Web of Science ®Google Scholar
• Stegmeier F, Amon A. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet. 2004;38:203–232. doi:10.1146/annurev.genet.38.072902.093051. PMID:15568976
   PubMed Web of Science ®Google Scholar
• Machín F, Torres-Rosell J, De Piccoli G, et al. Transcription of ribosomal genes can cause nondisjunction. J Cell Biol. 2006;173:893–903. doi:10.1083/jcb.200511129. PMID:16769819
   PubMed Web of Science ®Google Scholar
• Clemente-Blanco A, Mayán-Santos M, Schneider DA, et al. Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature. 2009;458:219–222. doi:10.1038/nature07652. PMID:19158678
   PubMed Web of Science ®Google Scholar
• Machín F, Quevedo O, Ramos-Pérez C, et al. Cdc14 phosphatase: warning, no delay allowed for chromosome segregation! Curr Genet. 2016;62:7–13. doi:10.1007/s00294-015-0502-1. PMID:26116076
   PubMed Web of Science ®Google Scholar
• Straight AF, Shou W, Dowd GJ, et al. Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell. 1999;97:245–256. doi:10.1016/S0092-8674(00)80734-5. PMID:10219245
   PubMed Web of Science ®Google Scholar
• Visintin R, Hwang ES, Amon A. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature. 1999;398:818–823. doi:10.1038/19775. PMID:10235265
   PubMed Web of Science ®Google Scholar
• Yoshida S, Asakawa K, Toh-e A. Mitotic exit network controls the localization of Cdc14 to the spindle pole body in Saccharomyces cerevisiae. Curr Biol. 2002;12:944–950. doi:10.1016/S0960-9822(02)00870-9. PMID:12062061
   PubMed Web of Science ®Google Scholar
• Stegmeier F, Visintin R, Amon A. Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase. Cell. 2002;108:207–220. doi:10.1016/S0092-8674(02)00618-9. PMID:11832211
   PubMed Web of Science ®Google Scholar
• Rahal R, Amon A. The Polo-like kinase Cdc5 interacts with FEAR network components and Cdc14. Cell Cycle. 2008;7:3262–3272. doi:10.4161/cc.7.20.6852. PMID:18927509
   PubMed Web of Science ®Google Scholar
• Liang F, Jin F, Liu H, et al. The molecular function of the yeast polo-like kinase Cdc5 in Cdc14 release during early anaphase. Mol Biol Cell. 2009;20:3671–3679. doi:10.1091/mbc.E08-10-1049. PMID:19570916
   PubMed Web of Science ®Google Scholar
• Shou W, Seol JH, Shevchenko A, et al. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell. 1999;97:233–244. doi:10.1016/S0092-8674(00)80733-3. PMID:10219244
   PubMed Web of Science ®Google Scholar
• Pereira G, Manson C, Grindlay J, et al. Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p. J Cell Biol. 2002;157:367–379. doi:10.1083/jcb.200112085. PMID:11970961
   PubMed Web of Science ®Google Scholar
• Weiss EL. Mitotic exit and separation of mother and daughter cells. Genetics. 2012;192:1165–1202. doi:10.1534/genetics.112.145516. PMID:23212898
   PubMed Web of Science ®Google Scholar
• Morano Ka, Grant CM, Moye-Rowley WS. The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics. 2012;190:1157–1195. doi:10.1534/genetics.111.128033. PMID:22209905
   PubMed Web of Science ®Google Scholar
• Ha CW, Huh WK. Rapamycin increases rDNA stability by enhancing association of Sir2 with rDNA in Saccharomyces cerevisiae. Nucleic Acids Res. 2011;39:1336–1350. doi:10.1093/nar/gkq895. PMID:20947565
   PubMed Web of Science ®Google Scholar
• Nishimura K, Fukagawa T, Takisawa H, et al. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods. 2009;6:917–922. doi:10.1038/nmeth.1401. PMID:19915560
   PubMed Web of Science ®Google Scholar
• Granot D, Snyder M. Segregation of the nucleolus during mitosis in budding and fission yeast. Cell Motil Cytoskeleton. 1991;20:47–54. doi:10.1002/cm.970200106. PMID:1661641
   PubMed Web of Science ®Google Scholar
• Morawska M, Ulrich HD. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast. 2013;30:341–351. doi:10.1002/yea.2967. PMID:23836714
   PubMed Web of Science ®Google Scholar
• Kalitsis P, Zhang T, Marshall KM, et al. Condensin, master organizer of the genome. Chromosom Res. 2017;25:61–76. doi:10.1007/s10577-017-9553-0.
   PubMed Web of Science ®Google Scholar
• Varela E, Shimada K, Laroche T, et al. Lte1, Cdc14 and MEN-controlled Cdk inactivation in yeast coordinate rDNA decompaction with late telophase progression. EMBO J. 2009;28:1562–1575. doi:10.1038/emboj.2009.111. PMID:19387493
   PubMed Web of Science ®Google Scholar
• Tong K, Skibbens RV. Pds5 regulators segregate cohesion and condensation pathways in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2015;112:7021–7026. doi:10.1073/pnas.1501369112. PMID:25986377
   PubMed Web of Science ®Google Scholar
• Wang B-D, Yong-Gonzalez V, Strunnikov AV. Cdc14p/FEAR pathway controls segregation of nucleolus in S. cerevisiae by facilitating condensin targeting to rDNA chromatin in anaphase. Cell Cycle. 2004;3:960–967. doi:10.4161/cc.3.7.1003. PMID:15190202
   PubMed Web of Science ®Google Scholar
• St-Pierre J, Douziech M, Bazile F, et al. Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell. 2009;34:416–426. doi:10.1016/j.molcel.2009.04.013. PMID:19481522
   PubMed Web of Science ®Google Scholar
• Walters AD, May CK, Dauster ES, et al. The yeast polo kinase Cdc5 regulates the shape of the mitotic nucleus. Curr Biol. 2014;24:2861–2867. doi:10.1016/j.cub.2014.10.029. PMID:25454593
   PubMed Web of Science ®Google Scholar
• Tomson BN, D'Amours D, Adamson BS, et al. Ribosomal DNA transcription-dependent processes interfere with chromosome segregation. Mol Cell Biol. 2006;26:6239–6247. doi:10.1128/MCB.00693-06. PMID:16880532
   PubMed Web of Science ®Google Scholar
• Villoria MT, Ramos F, Dueñas E, et al. Stabilization of the metaphase spindle by Cdc14 is required for recombinational DNA repair. EMBO J. 2017;36:79–101. doi:10.15252/embj.201593540. PMID:27852625
   PubMed Web of Science ®Google Scholar
• Shou W, Sakamoto KM, Keener J, et al. Net1 stimulates RNA polymerase I transcription and regulates nucleolar structure independently of controlling mitotic exit. Mol Cell. 2001;8:45–55. doi:10.1016/S1097-2765(01)00291-X. PMID:11511359
   PubMed Web of Science ®Google Scholar
• Takahara T, Maeda T. Transient Sequestration of TORC1 into Stress Granules during Heat Stress. Mol Cell. 2012;47:242–252. doi:10.1016/j.molcel.2012.05.019. PMID:22727621
   PubMed Web of Science ®Google Scholar
• Tsang CK, Bertram PG, Ai W, et al. Chromatin-mediated regulation of nucleolar structure and RNA Pol I localization by TOR. EMBO J. 2003;22:6045–6056. doi:10.1093/emboj/cdg578. PMID:14609951
   PubMed Web of Science ®Google Scholar
• Tsang CK, Li H, Zheng XS. Nutrient starvation promotes condensin loading to maintain rDNA stability. EMBO J. 2007;26:448–458. doi:10.1038/sj.emboj.7601488. PMID:17203076
   PubMed Web of Science ®Google Scholar
• Tsang CK, Zheng XFS. Opposing role of condensin and radiation-sensitive gene RAD52 in ribosomal DNA stability regulation. J Biol Chem. 2009;284:21908–21919. doi:10.1074/jbc.M109.031302. PMID:19520859
   PubMed Web of Science ®Google Scholar
• Loewith R, Hall MN. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics. 2011;189:1177–1201. doi:10.1534/genetics.111.133363. PMID:22174183
   PubMed Web of Science ®Google Scholar
• Trotter EW, Berenfeld L, Krause SA, et al. Protein misfolding and temperature up-shift cause G1 arrest via a common mechanism dependent on heat shock factor in Saccharomycescerevisiae. Proc Natl Acad Sci U S A. 2001;98:7313–7318. doi:10.1073/pnas.121172998. PMID:11416208
   PubMed Web of Science ®Google Scholar
• Trotter EW, Kao CM-F, Berenfeld L, et al. Misfolded proteins are competent to mediate a subset of the responses to heat shock in Saccharomyces cerevisiae. J Biol Chem. 2002;277:44817–44825. doi:10.1074/jbc.M204686200. PMID:12239211
   PubMedGoogle Scholar
• Bonfils G, Jaquenoud M, Bontron S, et al. Leucyl-tRNA Synthetase Controls TORC1 via the EGO Complex. Mol Cell. 2012;46:105–110. doi:10.1016/j.molcel.2012.02.009. PMID:22424774
   PubMed Web of Science ®Google Scholar
• Shen D, Skibbens RV. Temperature-dependent regulation of rDNA condensation in Saccharomyces cerevisiae. Cell Cycle. 2017;4101:00–00.
   Google Scholar
• Robellet X, Thattikota Y, Wang F, et al. A high-sensitivity phospho-switch triggered by Cdk1 governs chromosome morphogenesis during cell division. Genes Dev. 2015;29:426–439. doi:10.1101/gad.253294.114. PMID:25691469
   PubMed Web of Science ®Google Scholar
• Medvedik O, Lamming DW, Kim KD, et al. MSN2 and MSN4 link calorie restriction and TOR to sirtuin-mediated lifespan extension in Saccharomyces cerevisiae. PLoS Biol. 2007;5:e261. doi:10.1371/journal.pbio.0050261. PMID:17914901
   PubMed Web of Science ®Google Scholar
• Solís EJ, Pandey JP, Zheng X, et al. Defining the Essential Function of Yeast Hsf1 Reveals a Compact Transcriptional Program for Maintaining Eukaryotic Proteostasis. Mol Cell. 2016;63:60–71. doi:10.1016/j.molcel.2016.05.014. PMID:27320198
   PubMed Web of Science ®Google Scholar
• Urban J, Soulard A, Huber A, et al. Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell. 2007;26:663–674. doi:10.1016/j.molcel.2007.04.020. PMID:17560372
   PubMed Web of Science ®Google Scholar
• de los Santos-Velázquez AI, de Oya IG, Manzano-López J, et al. Late rDNA Condensation Ensures Timely Cdc14 Release and Coordination of Mitotic Exit Signaling with Nucleolar Segregation. Curr Biol. 2017;:1–16. PMID:27916526
   PubMed Web of Science ®Google Scholar
• Witkin KL, Chong Y, Shao S, et al. The budding yeast nuclear envelope adjacent to the nucleolus serves as a membrane sink during mitotic delay. Curr Biol. 2012;22:1128–1133. doi:10.1016/j.cub.2012.04.022. PMID:22658600
   PubMed Web of Science ®Google Scholar
• Grunstein M, Gasser SM. Epigenetics in Saccharomyces cerevisiae. Cold Spring Harb Perspect Biol. 2013;5. doi:10.1101/cshperspect.a017491. PMID:23818500
   PubMed Web of Science ®Google Scholar
• Li H, Tsang CK, Watkins M, et al. Nutrient regulates Tor1 nuclear localization and association with rDNA promoter. Nature. 2006;442:1058–1061. doi:10.1038/nature05020. PMID:16900101
   PubMed Web of Science ®Google Scholar
• Kos-Braun IC, Jung I, Koš M. Tor1 and CK2 kinases control a switch between alternative ribosome biogenesis pathways in a growth-dependent manner. PLOS Biol. 2017;15:e2000245. doi:10.1371/journal.pbio.2000245. PMID:28282370
   PubMed Web of Science ®Google Scholar
• Rodriguez-Rodriguez JA, Moyano Y, Játiva S, et al. Mitotic Exit Function of Polo-like Kinase Cdc5 Is Dependent on Sequential Activation by Cdk1. Cell Rep. 2016;15:2050–2062. doi:10.1016/j.celrep.2016.04.079. PMID:27210759
   PubMed Web of Science ®Google Scholar
• Mallory M, Gogineni E, Jones GC, et al. Therapeutic hyperthermia: The old, the new, and the upcoming. Crit Rev Oncol Hematol. 2016;97:56–64. doi:10.1016/j.critrevonc.2015.08.003. PMID:26315383
   PubMed Web of Science ®Google Scholar
• Hein N, Hannan KM, George AJ, et al. The nucleolus: An emerging target for cancer therapy. Trends Mol Med. 2013;19:643–654. doi:10.1016/j.molmed.2013.07.005. PMID:23953479
   PubMed Web of Science ®Google Scholar
• Dokladny K, Myers OB, Moseley PL. Heat shock response and autophagy—Cooperation and control. Autophagy. 2015;11:200–213. doi:10.1080/15548627.2015.1009776. PMID:25714619
   PubMed Web of Science ®Google Scholar
• Smith JS, Burke DJ. Yeast Genetics: Methods and Protocols. New York, NY: Springer New York; 2014.
   Google Scholar
• Kushnirov VV. Rapid and reliable protein extraction from yeast. Yeast. 2000;16:857–860. doi:10.1002/1097-0061(20000630)16:9%3c857::AID-YEA561%3e3.0.CO;2-B. PMID:10861908
   PubMed Web of Science ®Google Scholar
• Quevedo O, García-Luis J, Matos-Perdomo E, et al. Nondisjunction of a single chromosome leads to breakage and activation of DNA damage checkpoint in g2. PLoS Genet. 2012;8:e1002509. doi:10.1371/journal.pgen.1002509. PMID:22363215
   PubMed Web of Science ®Google Scholar
• García-Luis J, Machín F. Mus81-Mms4 and Yen1 resolve a novel anaphase bridge formed by noncanonical Holliday junctions. Nat Commun. 2014;5:5652. doi:10.1038/ncomms6652. PMID:25466415
   PubMed Web of Science ®Google Scholar