Interlinked bistable mechanisms generate robust mitotic transitions

References

• Mochida S, Rata S, Hino H, Nagai T, Novák B. Two Bistable Switches Govern M Phase Entry. Curr Biol. 2016;26:3361-3367. doi:10.1016/j.cub.2016.10.022. PMID:27889260
   PubMed Web of Science ®Google Scholar
• Mirkovic M, Hutter LH, Novák B, Oliveira RA. Premature sister chromatid separation is poorly detected by the spindle assembly checkpoint as a result of system-level feedback. Cell Rep. 2015;13:469-478. doi:10.1016/j.celrep.2015.09.020
   PubMed Web of Science ®Google Scholar
• Morgan D. The cell cycle: Principles of control. London (UK): New Science Press, 2007.
   Google Scholar
• Tyson JJ, Novak B. Irreversible transitions, bistability and checkpoint controls in the eukaryotic cell cycle: A systems-level understanding. In: Walhout M, Vidal M, Dekker J, editors. Handbook of systems biology. Amsterdam: Elsevier; 2013 p.265-285.
   Google Scholar
• Errico A, Deshmukh K, Tanaka Y, Pozniakovsky A, Hunt T. Identification of substrates for cyclin dependent kinases. Adv Enzyme Regul. 2010;50:375-399. doi:10.1016/j.advenzreg.2009.12.001. PMID:20045433
   PubMedGoogle Scholar
• Schmitz M, Held M, Janssens V, Hutchins JR, Hudecz O, Ivanova E, Goris J, Trinkle-Mulcahy L, Lamond AI, Poser I, et al. Live-cell imaging RNAi screen identifies PP2A-B55alpha and importin-beta1 as key mitotic exit regulators in human cells. Nat Cell Biol. 2010;12:886-93. doi:10.1038/ncb2092. PMID:20711181
   PubMed Web of Science ®Google Scholar
• Godfrey M, Touati SA, Kataria M, Jones A, Snijders AP, Uhlmann F. PP2ACdc55 Phosphatase imposes ordered cell-cycle phosphorylation by opposing threonine phosphorylation. Mol Cell. 2017;65:393-402. e3. doi:10.1016/j.molcel.2016.12.018. PMID:28132839
   PubMed Web of Science ®Google Scholar
• Cundell M., Hutter LH, Nunes Bastos R, Poser E, Holder J, Mohammed S, Novak B, Barr FA. A PP2A-B55 recognition signal controls substrate dephosphorylation kinetics during mitotic exit. J Cell Biol. 2016;214:539-54. doi:10.1083/jcb.201606033. PMID:27551054
   PubMed Web of Science ®Google Scholar
• Evans T, Rosenthal E, Youngblom J, Distel D, Hunt T. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 1983;33:389-96. doi:10.1016/0092-8674(83)90420-8. PMID:6134587
   PubMed Web of Science ®Google Scholar
• Parker L, Piwnica-Worms H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science. 1992;257:1955-7. doi:10.1126/science.1384126. PMID:1384126
   PubMed Web of Science ®Google Scholar
• Mueller PR, Coleman TR, Kumagai A, Dunphy WG. Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science. 1995;270:86-90. doi:10.1126/science.270.5233.86. PMID:7569953
   PubMed Web of Science ®Google Scholar
• Welburn J, Tucker JA, Johnson T, Lindert L, Morgan M, Willis A, Noble ME, Endicott JA. How tyrosine 15 phosphorylation inhibits the activity of cyclin-dependent kinase 2-cyclin A. J Biol Chem. 2007;282:3173-81. doi:10.1074/jbc.M609151200. PMID:17095507
   PubMed Web of Science ®Google Scholar
• Tang Z, Coleman T, Dunphy W. Two distinct mechanisms for negative regulation of the Wee1 protein kinase. EMBO J. 1993;12:3427-36 PMID:7504624
   PubMed Web of Science ®Google Scholar
• Strausfeld U, Labbé JC, Fesquet D, Cavadore JC, Picard A, Sadhu K, Russell P, Dorée M. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein. Nature. 1991;351:242-5. doi:10.1038/351242a0. PMID:1828290
   PubMed Web of Science ®Google Scholar
• Izumi T, Maller J. Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol Biol Cell. 1993;4:1337-50. doi:10.1091/mbc.4.12.1337. PMID:7513216
   PubMed Web of Science ®Google Scholar
• Novak B, Tyson J. Numerical analysis of a comprehensive model of M-phase control in Xenopus oocyte extracts and intact embryos. J Cell Sci. 1993;106:1153-68 PMID:8126097
   PubMed Web of Science ®Google Scholar
• Sha W, Moore J, Chen K, Lassaletta AD, Yi CS, Tyson JJ, Sible JC. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc Natl Acad Sci U A 2003;100:975-80. doi:10.1073/pnas.0235349100.
   PubMed Web of Science ®Google Scholar
• Pomerening J, Sontag E, Ferrell JJ. Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat Cell Biol 2003;5:346-51. doi:10.1038/ncb954. PMID:12629549
   PubMed Web of Science ®Google Scholar
• Mochida S, Ikeo S, Gannon J, Hunt T. Regulated activity of PP2A-B55 delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 2009;28:2777-85. doi:10.1038/emboj.2009.238. PMID:19696736
   PubMed Web of Science ®Google Scholar
• Hunt T. On the regulation of protein phosphatase 2A and its role in controlling entry into and exit from mitosis. Adv Biol Regul. 2013;53:173-8. doi:10.1016/j.jbior.2013.04.001. PMID:23672858
   PubMedGoogle Scholar
• Mochida S, Maslen S, Skehel M, Hunt T. Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science. 2010;330:1670-3. doi:10.1126/science.1195689. PMID:21164013
   PubMed Web of Science ®Google Scholar
• Gharbi-Ayachi A, Labbé JC, Burgess A, Vigneron S, Strub JM, Brioudes E, Van-Dorsselaer A, Castro A, Lorca T. The substrate of greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science. 2010;330:1673-7. doi:10.1126/science.1197048. PMID:21164014
   PubMed Web of Science ®Google Scholar
• Yu J, Zhao Y, Li Z, Galas S Goldberg ML. Greatwall kinase participates in the Cdc2 autoregulatory loop in Xenopus egg extracts. Mol Cell 2006;22:83-91. doi:10.1016/j.molcel.2006.02.022. PMID:16600872
   PubMed Web of Science ®Google Scholar
• Williams BC, Filter JJ, Blake-Hodek KA, Wadzinski BE, Fuda NJ, Shalloway D, Goldberg ML. Greatwall-phosphorylated Endosulfine is both an inhibitor and a substrate of PP2A-B55 heterotrimers. eLife 2014;3:e01695. doi:10.7554/eLife.01695. PMID:24618897
   PubMed Web of Science ®Google Scholar
• Kishimoto T. Entry into mitosis: a solution to the decades-long enigma of MPF. Chromosoma. 2015;124:417-28. doi:10.1007/s00412-015-0508-y. PMID:25712366
   PubMed Web of Science ®Google Scholar
• Vigneron S, Brioudes E, Burgess A, Labbé JC, Lorca T, Castro A. Greatwall maintains mitosis through regulation of PP2A. EMBO J. 2009;28:2786-2793. doi:10.1038/emboj.2009.228. PMID:19680222
   PubMed Web of Science ®Google Scholar
• Cundell MJ, Bastos RN, Zhang T, Holder J, Gruneberg U, Novak B, Barr FA. The BEG (PP2A-B55/ENSA/Greatwall) pathway ensures cytokinesis follows chromosome separation. Mol Cell. 2013;52:393-405. doi:10.1016/j.molcel.2013.09.005. PMID:24120663
   PubMed Web of Science ®Google Scholar
• Vinod P, Novak B. Model scenarios for switch-like mitotic transitions. FEBS Lett. 2015;589:667-71. doi:10.1016/j.febslet.2015.02.007. PMID:25683003
   PubMed Web of Science ®Google Scholar
• Rogers S, Fey D, McCloy RA, Parker BL, Mitchell NJ, Payne RJ, Daly RJ, James DE, Caldon CE, Watkins DN, et al. PP1 initiates the dephosphorylation of MASTL, triggering mitotic exit and bistability in human cells. J Cell Sci. 2016;129:1340-1354. doi:10.1242/jcs.179754. PMID:26872783
   PubMed Web of Science ®Google Scholar
• Ma S, Vigneron S, Robert P, Strub JM, Cianferani S, Castro A, Lorca T. Greatwall dephosphorylation and inactivation upon mitotic exit is triggered by PP1. J. Cell Sci. 2016;129:1329-1339. doi:10.1242/jcs.178855. PMID:26906418
   PubMed Web of Science ®Google Scholar
• Cardelli L, Csikász-Nagy A. The cell cycle switch computes approximate majority. Sci Rep. 2012;2:656. doi:10.1038/srep00656. PMID:22977731
   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
• Uchida KS, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T. Kinetochore stretching inactivates the spindle assembly checkpoint. J. Cell Biol. 2009;184:383-390. doi:10.1083/jcb.200811028. PMID:19188492
   PubMed Web of Science ®Google Scholar
• Maresca TJ, Salmon ED. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J Cell Biol. 2009;184:373-381. doi:10.1083/jcb.200808130. PMID:19193623
   PubMed Web of Science ®Google Scholar
• Rieder CL. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol. 1995;130:941-948. doi:10.1083/jcb.130.4.941. PMID:7642709
   PubMed Web of Science ®Google Scholar
• Musacchio A. The molecular biology of spindle assembly checkpoint signaling dynamics. Curr Biol. 2015;25:R1002-18. doi:10.1016/j.cub.2015.08.051. PMID:26485365
   PubMed Web of Science ®Google Scholar
• Mirchenko L, Uhlmann F. Sli15INCENP Dephosphorylation prevents mitotic checkpoint reengagement due to loss of tension at anaphase onset. Curr Biol. 2010;20:1396-1401. doi:10.1016/j.cub.2010.06.023. PMID:20619650
   PubMed Web of Science ®Google Scholar
• Oliveira RA, Hamilton RS, Pauli A, Davis I, Nasmyth K. Cohesin cleavage and Cdk inhibition trigger formation of daughter nuclei. Nat Cell Biol. 2010;12:185-192. doi:10.1038/ncb2018. PMID:20081838
   PubMed Web of Science ®Google Scholar
• Tsukahara T, Tanno Y, Watanabe Y. Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature. 2010;467:719-723. doi:10.1038/nature09390. PMID:20739936
   PubMed Web of Science ®Google Scholar
• Vázquez-Novelle MD, Petronczki M. Relocation of the chromosomal passenger complex prevents mitotic checkpoint engagement at anaphase. Curr Biol. 2010;20:1402-1407. doi:10.1016/j.cub.2010.06.036. PMID:20619651
   PubMed Web of Science ®Google Scholar
• Rattani A, Vinod PK, Godwin J, Tachibana-Konwalski K, Wolna M, Malumbres M, Novák B, Nasmyth K. Dependency of the spindle assembly checkpoint on Cdk1 renders the anaphase transition irreversible. Curr Biol. 2014;24:630-637. doi:10.1016/j.cub.2014.01.033. PMID:24583015
   PubMed Web of Science ®Google Scholar
• Vázquez-Novelle MD, Sansregret L, Dick AE, Smith CA, McAinsh AD, Gerlich DW, Petronczki M. Cdk1 inactivation terminates mitotic checkpoint surveillance and stabilizes kinetochore attachments in anaphase. Curr Biol. 2014;24:638-645. doi:10.1016/j.cub.2014.01.034. PMID:24583019
   PubMed Web of Science ®Google Scholar
• Dick AE, Gerlich DW. Kinetic framework of spindle assembly checkpoint signalling. Nat Cell Biol. 2013;15:1370-1377. doi:10.1038/ncb2842. PMID:24096243
   PubMed Web of Science ®Google Scholar
• Ferrell JE. Feedback regulation of opposing enzymes generates robust all-or-none bistable responses. Curr Biol. 2008;18:R244-R245. doi:10.1016/j.cub.2008.02.035. PMID:18364225
   PubMed Web of Science ®Google Scholar