The biochemistry of mitosis

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 3, 2015, Pages

  Wieser, Samuel ^a   Pines, Jonathon ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA;

CYCLIN DEPENDENT KINASE; PHOSPHOPROTEIN PHOSPHATASE;

ANIMAL; BIOCHEMISTRY; METABOLISM; MITOSIS; PHYSIOLOGY; SIGNAL TRANSDUCTION; SISTER CHROMATID EXCHANGE; YEAST;

ANIMALS; BIOCHEMICAL PROCESSES; CYCLIN-DEPENDENT KINASES; MITOSIS; PHOSPHOPROTEIN PHOSPHATASES; SIGNAL TRANSDUCTION; SISTER CHROMATID EXCHANGE; YEASTS;

EID: 84924769262     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a015776     Document Type: Article

References (160)

1. Amon A, Surana U, Muroff I, Nasmyth K. 1992. Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature 355: 368-371.
2. Atherton-Fessler S, Parker LL, Geahlen RL, Piwnica-Worms H. 1993. Mechanisms of p34cdc2 regulation. Mol Cell Biol 13: 1675-1685.
3. Atkin J, Halova L, Ferguson J, Hitchin JR, Lichawska-Cieslar A, Jordan AM, Pines J, Wellbrock C, Petersen J. 2014. Torin1-mediated TOR kinase inhibition reduces Wee1 levels and advances mitotic commitment in fission yeast and HeLa cells. J Cell Sci 127: 1346-1356.
4. Barford D. 2011. Structural insights into anaphase-promoting complex function and mechanism. Philos Trans R Soc Lond B Biol Sci 366: 3605-3624.
5. Bayliss R, Sardon T, Vernos I, Conti E. 2003. Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol Cell 12: 851-862.
6. Blake-Hodek KA, Williams BC, Zhao Y, Castilho PV, Chen W, Mao Y, Yamamoto TM, Goldberg ML. 2012. Determinants for activation of the atypical AGC kinase Greatwall during M phase entry. Mol Cell Biol 32: 1337-1353.
7. Bollen M, Gerlich DW, Lesage B. 2009. Mitotic phosphatases: From entry guards to exit guides. Trends Cell Biol 19: 531-541.
8. Bollen M, Peti W, Ragusa MJ, Beullens M. 2010. The extended PP1 toolkit: Designed to create specificity. Trends Bio-chem Sci 35: 450-458.
9. Bourne Y, Arvai AS, Bernstein SL, Watson MH, Reed SI, Endicott JE, Noble ME, Johnson LN, Tainer JA. 1995. Crystal structure of the cell cycle-regulatory protein suc1 reveals a (3-hinge conformational switch). Proc Natl Acad Sci 92: 10232-10236.
10. Brown NR, Noble ME, Endicott JA, Garman EF, Wakatsuki S, Mitchell E, Rasmussen B, Hunt T, Johnson LN. 1995. The crystal structure of cyclin A. Structure 3: 1235-1247.
11. Brown NR, Noble ME, Lawrie AM, Morris MC, Tunnah P, Divita G, Johnson LN, Endicott JA. 1999. Effects of phosphorylation of threonine 160 on cyclin-dependent kinase 2 structure and activity. J Biol Chem 274: 8746-8756.
12. Burton JL, Solomon MJ. 2007. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev 21: 655-667.
13. Buschhorn BA, Petzold G, Galova M, Dube P, Kraft C, Her-zog F, Stark H, Peters JM. 2011. Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1. Nat Struct Mol Biol 18: 6-13.
14. Carazo-Salas RE, Guarguaglini G, Gruss OJ, Segref A, Kar-senti E, Mattaj IW. 1999. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400: 178-181.
15. Chang L, Zhang Z, Yang J, McLaughlin SH, Barford D. 2014. Molecular architecture and mechanism of the anaphase-promoting complex. Nature 513: 388-393.
16. Chao WC, Kulkarni K, Zhang Z, Kong EH, Barford D. 2012. Structure of the mitotic checkpoint complex. Nature 484: 208-213.
17. Cheeseman IM. 2014. The kinetochore. Cold Spring Harb Perspect Biol 6: a015826.
18. Chen MS, Hurov J, White LS, Woodford-Thomas T, Piwni-ca-Worms H. 2001. Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol Cell Biol 21: 3853-3861.
19. Chen F, Archambault V, Kar A, Lio P, D’Avino PP, Sinka R, Lilley K, Laue ED, Deak P, Capalbo L, et al. 2007. Multiple protein phosphatases are required for mitosis in Dro-sophila. Curr Biol 17: 293-303.
20. Ciechanover A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79: 13-21.
21. Clute P, Pines J. 1999. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1: 82-87.
22. Collin P, Nashchekina O, Walker R, Pines J. 2013. The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat Cell Biol 15: 1378-1385.
23. Coudreuse D, Nurse P. 2010. Driving the cell cycle with a minimal CDK control network. Nature 468: 1074-1079.
24. Cundell MJ, Bastos RN, Zhang T, Holder J, Gruneberg U, Novak B, Barr FA. 2013. The BEG (PP2A-B55/ENSA/ Greatwall) pathway ensures cytokinesis follows chromosome separation. Mol Cell 52: 393-405.
25. da Fonseca PCA, Kong EH, Zhang Z, Schreiber A, Williams MA, Morris EP, Barford D. 2011. Structures of APC/ CCdh1 with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470: 274-278.
26. D’Amours D, Amon A. 2004. At the interface between signaling and executing anaphase—Cdc14 and the FEAR network. Genes Dev 18: 2581-2595.
27. D’Avino PP, Giansanti MG, Petronczki M. 2015. Cytokinesis in animal cells. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a015834.
28. De Antoni A, Pearson CG, Cimini D, Canman JC, Sala V, Nezi L, Mapelli M, Sironi L, Faretta M, Salmon ED, et al. 2005. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr Biol 15: 214-225.
29. den Elzen N, Pines J. 2001. Cyclin A is destroyed in pro-metaphase and can delay chromosome alignment and anaphase. J Cell Biol 153: 121-136.
30. Dick AE, Gerlich DW. 2013. Kinetic framework of spindle assembly checkpoint signalling. Nat Cell Biol 15: 1370-1377.
31. Di Fiore B, Pines J. 2010. How cyclin A destruction escapes the spindle assembly checkpoint. J Cell Biol 190: 501-509.
32. Errico A, Deshmukh K, Tanaka Y, Pozniakovsky A, Hunt T. 2010. Identification of substrates for cyclin dependent kinases. Adv Enzyme Regul 50: 375-399.
33. Eytan E, Wang K, Miniowitz-Shemtov S, Sitry-Shevah D, Kaisari S, Yen TJ, Liu S-T, Hershko A. 2014. Disassembly of mitotic checkpoint complexesby the joint action ofthe AAA-ATPase TRIP13 and pp31comet. Proc Natl Acad Sci 111: 12019-12024.
34. Ferguson AM, White LS, Donovan PJ, Piwnica-Worms H. 2005. Normal cell cycle and checkpoint responsesin mice and cells lacking Cdc25B and Cdc25C protein phospha-tases. Mol Cell Biol 25: 2853-2860.
35. Floyd S, Pines J, Lindon C. 2008. APC/C Cdh1 targets aurora kinase to control reorganization of the mitotic spindle at anaphase. Curr Biol 18: 1649-1658.
36. Foster SA, Morgan DO. 2012. The APC/C subunit Mnd2/ Apc15 promotes Cdc20 autoubiquitination and spindle assembly checkpoint inactivation. Mol Cell 47: 921-932.
37. Francis D. 2011. A commentary on the G2/M transition of the plant cell cycle. Ann Bot 107: 1065-1070.
38. Furuno N, den Elzen N, Pines J. 1999. Human cyclin A is required for mitosis until mid-prophase. J Cell Biol 147: 295-306.
39. Garnett MJ, Mansfeld J, Godwin C, Matsusaka T, Wu J, Russell P, Pines J, Venkitaraman AR. 2009. UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nat Cell Biol 11: 1363-1369.
40. Gavet O, Pines J. 2010a. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J Cell Biol 189: 247-259.
41. Gavet O, Pines J. 2010b. Progressive activation of cyclin B1-Cdk1 coordinates entry to mitosis. Dev Cell 18: 533-543.
42. Geley S, Kramer E, Gieffers C, Gannon J, Peters JM, Hunt T. 2001. APC/C-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J Cell Biol 153: 137-148.
43. Gharbi-Ayachi A, Labbé J.-C, Burgess A, Vigneron S, Strub J-M, Brioudes E, Van-Dorsselaer A, Castro A, Lorca T. 2010. The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science 330: 1673-1677.
44. Glotzer M, Murray AW, Kirschner MW. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138.
45. Grallert A, Patel A, Tallada VA, Chan KY, Bagley S, Krapp A, Simanis V, Hagan IM. 2013. Centrosomal MPF triggers the mitotic and morphogenetic switches of fission yeast. Nat Cell Biol 15: 88-95.
46. Gruss OJ, Carazo-Salas RE, Schatz CA, Guarguaglini G, Kast J, Wilm M, Le Bot N, Vernos I, Karsenti E, Mattaj IW. 2001. Ran induces spindle assembly by reversing the inhibitory effect of importin a on TPX2 activity. Cell 104: 83-93.
47. Güttler T, Görlich D. 2011. Ran-dependent nuclear export mediators: A structural perspective. EMBO J 30: 3457-3474.
48. Habu T, Kim SH, Weinstein J, Matsumoto T. 2002. Identification of a MAD2-binding protein, CMT2, and its role in mitosis. EMBO J 21: 6419-6428.
49. Hagting A, Karlsson C, Clute P, Jackman M, Pines J. 1998. MPF localisation is controlled bynuclear export. EMBO J 17: 4127-4138.
50. Hagting A, den Elzen N, Vodermaier HC, Waizenegger IC, Peters J-M, Pines J. 2002. Human securin proteolysis is controlled by the spindle checkpoint and reveals when the APC/C switches from activation by Cdc20 to Cdh1. J Cell Biol 157: 1125-1137.
51. Hames RS, Wattam SL, Yamano H, Bacchieri R, Fry AM. 2001. APC/C-mediated destruction of the centrosomal kinase Nek2A occurs inearly mitosis and depends upon a cyclin A-type D-box. EMBO J 20: 7117-7127.
52. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM. 2005. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 3: e69.
53. Hayes MJ, Kimata Y, Wattam SL, Lindon C, Mao G, Yamano H, Fry AM. 2006. Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat Cell Biol 8: 607-614.
54. He J, Chao WCH, Zhang Z, Yang J, Cronin N, Barford D. 2013. Insights into degron recognition by APC/C coac-tivators from the structure of an Acm1-Cdh1 complex. Mol Cell 50: 649-660.
55. Heroes E, Lesage B, Görnemann J, Beullens M, Van Meervelt L, Bollen M. 2013. The PP1 binding code: A molecular-lego strategy that governs specificity. FEBS J 280: 584-595.
56. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem 67: 425-479.
57. Hirano T. 2015. Chromosome dynamics during mitosis. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect. a015792.
58. Holland AJ, Taylor SS. 2006. Cyclin-B1-mediated inhibition of excess separase is required for timely chromosome disjunction. J Cell Sci 119: 3325-3336.
59. Hoyt MA, Trotis L, Roberts BT. 1991. S. cerevisiae genes required for cell cycle arrest in response to loss of micro-tubule function. Cell 66: 507-517.
60. Huang X, Andreu-Vieyra CV, York JP, Hatcher R, Lu T, Mat-zuk MM, Zhang P. 2008. Inhibitory phosphorylation of separase is essential for genome stability and viability of murine embryonic germ cells. PLoS Biol 6: e15.
61. Izawa D, Pines J. 2011. How APC/C-Cdc20 changes its substrate specificity in mitosis. Nat Cell Biol 13: 223-233.
62. Izawa D, Pines J. 2012. Mad2 and the APC/C compete for the same site on Cdc20 to ensure proper chromosome segregation. J Cell Biol 199: 27-37.
63. Jackman M, Kubota Y, den Elzen N, Hagting A, Pines J. 2002. Cyclin A-and cyclin E-Cdk complexes shuttle between the nucleus and the cytoplasm. Mol Biol Cell 13: 1030-1045.
64. Jackman M, Lindon C, Nigg EA, Pines J. 2003. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 5: 143-148.
65. Jacobs HW, Knoblich JA, Lehner CF. 1998. Drosophila cyclin B3 is required for female fertility and is dispensable for mitosis like cyclin B. Genes Dev 12: 3741-3751.
66. Jeffrey PD, Russo AA, Polyak K, Gibbs E, Hurwitz J, Mas-sague J, Pavletich NP. 1995. Structureof acyclinA-CDK2 complex. Nature 376: 313-320.
67. Juanes MA, Khoueiry R, Kupka T, Castro A, Mudrak I, Ogris E, Lorca T, Piatti S. 2013. Budding yeast Greatwall and endosulfines control activity and spatial regulation of PP2ACdc55 for timely mitotic progression. PLoS Genet 9: e1003575.
68. Kabeche L, Compton DA. 2013. Cyclin A regulates kineto-chore microtubules to promote faithful chromosome segregation. Nature 502: 110-113.
69. Kalab P, Pu RT, Dasso M. 1999. The ran GTPase regulates mitotic spindle assembly. Curr Biol 9: 481-484.
70. Kim SY, Ferrell JEJ. 2007. Substrate competition as a source of ultrasensitivity in the inactivation of Wee1. Cell 128: 1133-1145.
71. Kinoshita N, Ohkura H, Yanagida M. 1990. Distinct, essential roles of type 1 and 2A protein phosphatases in the control of the fission yeast cell division cycle. Cell 63: 405-415.
72. Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y. 2006. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441: 46-52.
73. Knoblich JA, Lehner CF. 1993. Synergistic action of Dro-sophila cyclins A and B during the G2-M transition. EMBO J 12: 65-74.
74. Kraft C, Herzog F, Gieffers C, Mechtler K, Hagting A, Pines J, Peters J.-M. 2003. Mitotic regulation of the human ana-phase-promoting complex by phosphorylation. EMBO J 22: 6598-6609.
75. Kraft C, Vodermaier HC, Maurer-Stroh S, Eisenhaber F, Peters JM. 2005. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol Cell 18: 543-553.
76. Kufer TA, Sillje HH, Korner R, Gruss OJ, Meraldi P, Nigg EA. 2002. Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 158: 617-623.
77. Kulukian A, Han JS, Cleveland DW. 2009. Unattached ki-netochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev Cell 16: 105-117.
78. Kumagai A, Dunphy WG. 1992. Regulation of the cdc25 protein during the cell cycle in Xenopus extracts. Cell 70: 139-151.
79. Labit H, Fujimitsu K, Bayin NS, Takaki T, Gannon J, Yamano H. 2012. Dephosphorylation of Cdc20 is required for its C-box-dependent activation of the APC/C. EMBO J 31: 3351-3362.
80. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A, Clevers H, Medema RH. 2005. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 7: 126-136.
81. Lara-Gonzalez P, Westhorpe FG, Taylor SS. 2012. The spindle assembly checkpoint. Curr Biol 22: R966-R980.
82. Lee G, White LS, Hurov KE, Stappenbeck TS, Piwnica-Worms H. 2009. Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proc Natl Acad Sci 106: 4701-4706.
83. Lenart P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM. 2007. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic rolesof Polo-like kinase1.Curr Biol 17: 304-315.
84. Lew DJ, Reed SI. 1995. A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J Cell Biol 129: 739-749.
85. Li R, Murray AW. 1991. Feedback control of mitosis in budding yeast. Cell 66: 519-531.
86. Li X, Nicklas RB. 1995. Mitotic forces control a cell-cycle checkpoint. Nature 373: 630-632.
87. Lindon C, Pines J. 2004. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J Cell Biol 164: 233-241.
88. Lindqvist A, van Zon W, Karlsson Rosenthal C, Wolthuis RM. 2007. Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol 5: e123.
89. Listovsky T, Zor A, Laronne A, Brandeis M. 2000. Cdk1 is essential for mammalian cyclosome/APC regulation. Exp Cell Res 255: 184-191.
90. Lowery DM, Clauser KR, Hjerrild M, Lim D, Alexander J, Kishi K, Ong SE, Gammeltoft S, Carr SA, Yaffe MB. 2007. Proteomic screen defines the Polo-box domain interac-tome and identifies Rock2asaPlk1 substrate. EMBO J 26: 2262-2273.
91. Mailand N, Podtelejnikov AV, Groth A, Mann M, Bartek J, Lukas J. 2002. Regulation of G2/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 21: 5911-5920.
92. Manchado E, Guillamot M, de Cárcer G, Eguren M, Trickey M, García-Higuera I, Moreno S, Yamano H, Cañamero M, Malumbres M. 2010. Targeting mitotic exit leads to tumor regression in vivo: Modulation by Cdk1, Mastl, and the PP2A/B55a,d phosphatase. Cancer Cell 18: 641-654.
93. Mansfeld J, Collin P, Collins MO, Choudhary J, Pines J. 2011. APC15 drives the turnover of MCC-CDC20 to make the spindle assembly checkpoint responsive to ki-netochore attachment. Nat Cell Biol 13: 1234-1243.
94. Matyskiela ME, Morgan DO. 2009. Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism. Mol Cell 34: 68-80.
95. McCleland ML, Farrell JA, O’Farrell PH. 2009. Influence of cyclin type and dose on mitotic entry and progression in the early Drosophila embryo. J Cell Biol 184: 639-646.
96. Mocciaro A, Schiebel E. 2010. Cdc14: A highly conserved family of phosphatases with non-conserved functions? J Cell Sci 123: 2867-2876.
97. Mocciaro A, Berdougo E, Zeng K, Black E, Vagnarelli P, Earnshaw W, Gillespie D, Jallepalli P, Schiebel E. 2010. Vertebrate cells genetically deficient for Cdc14A or Cdc14B retain DNA damage checkpoint proficiency but are impaired in DNA repair. J Cell Biol 189: 631-639.
98. Mochida S, Ikeo S, Gannon J, Hunt T. 2009. Regulated activity of PP2A-B55 d is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J 28: 2777-2785.
99. Mochida S, Maslen SL, Skehel M, Hunt T. 2010. Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science 330: 1670-1673.
100. Muhlhausser P, Kutay U. 2007. An invitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown. J Cell Biol 178: 595-610.
101. Nigg EA. 1991. The substrates of the cdc2 kinase. Semin Cell Biol 2: 261-270.
102. Nigg EA. 1993. Cellular substrates of p34cdc2 and its companion cyclin-dependent kinases. Trends Cell Biol 3:296-301.
103. Nurse P. 1990. Universal control mechanism regulating onset of M-phase. Nature 344: 503-508.
104. Okumura E, Morita A, Wakai M, Mochida S, Hara M, Ki-shimoto T. 2014. Cyclin B-Cdk1 inhibits protein phos-phatase PP2A-B55 via a Greatwall kinase-independent mechanism. J Cell Biol 204: 881-889.
105. Ookata K, Hisanaga S, Okano T, Tachibana K, Kishimoto T. 1992. Relocation and distinct subcellular localization of p34cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO J 11: 1763-1772.
106. Pagliuca FW, Collins MO, Lichawska A, Zegerman P, Choudhary JS, Pines J. 2011. Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol Cell 43: 406-417.
107. Passmore LA, Barford D. 2005. Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition. EMBO Rep 6: 873-878.
108. Passmore LA, McCormack EA, Au SW, Paul A, Willison KR, Harper JW, Barford D. 2003. Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J 22: 786-796.
109. Patra D, Wang SX, Kumagai A, Dunphy WG. 1999. The Xenopus Suc1/Cks protein promotes the phosphoryla-tion of G2/M regulators. J Biol Chem 274: 36839-36842.
110. Pavletich NP. 1999. Mechanisms of cyclin-dependent kinase regulation: Structures of Cdks, their cyclin activators, and Cip and INK4 inhibitors. J Mol Biol 287: 821-828.
111. Petersen J, Nurse P. 2007. TOR signalling regulates mitotic commitment through the stress MAP kinase pathway and the Polo and Cdc2 kinases. Nat Cell Biol 9: 1263-1272.
112. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
113. Pines J. 2006. Mitosis: A matter of getting rid of the right protein at the right time. Trends Cell Biol 16: 55-63.
114. Pines J. 2011. Cubism and the cell cycle: The many faces of the APC/C. Nat Rev Mol Cell Biol 12: 427-438.
115. Pines J, Hagan I. 2011. The Renaissance or the cuckoo clock. Philos Trans R Soc Lond B Biol Sci 366: 3625-3634.
116. Pines J, Hunter T. 1991. Human cyclins A and B are differentially located in the cell and undergo cell cycle dependent nuclear transport. J Cell Biol 115: 1-17.
117. Rangone H, Wegel E, Gatt MK, Yeung E, Flowers A, Debski J, Dadlez M, Janssens V, Carpenter ATC, Glover DM. 2011.Suppression of scant identifies Endos as a substrate of Greatwall kinase andanegative regulatorofprotein phos-phatase 2A in mitosis. PLoS Genet 7: e1002225.
118. Reber S, Hyman AA. 2015. Emergent propertiesof the meta-phase spindle. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a015784.
119. Reddy SK, Rape M, Margansky WA, Kirschner MW. 2007. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 446: 921-925.
120. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, et al. 2006. Protein phosphatase 2A protects centromeric sister chro-matid cohesion during meiosis I. Nature 441: 53-61.
121. Rieder CL, Cole RW, Khodjakov A, Sluder G. 1995. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130: 941-948.
122. Rock JM, Amon A. 2009. The FEAR network. Curr Biol 19: R1063-R1068.
123. Rodrigo-Brenni MC, Morgan DO. 2007. Sequential E2s drive polyubiquitin chain assembly on APC targets. Cell 130: 127-139.
124. Rudner AD, Murray AW. 2000. Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex. J Cell Biol 149: 1377-1390.
125. Russo AA, Jeffrey PD, Pavletich NP. 1996. Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat Struct Biol 3: 696-700.
126. Santos SD, Wollman R, Meyer T, Ferrell JEJ. 2012. Spatial positive feedback at the onset of mitosis. Cell 149: 1500-1513.
127. Schöckel L, Möckel M, Mayer B, Boos D, Stemmann O.2011. Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat Cell Biol 13: 966-972.
128. Siomos MF, Badrinath A, Pasierbek P, Livingstone D, White J, Glotzer M, Nasmyth K. 2001. Separase is required for chromosome segregation during meiosis I in Caenorhab-ditis elegans. Curr Biol 11: 1825-1835.
129. Steen RL, Martins SB, Tasken K, Collas P. 2000. Recruitment of protein phosphatase 1 to the nuclear envelope by A-kinase anchoring protein AKAP149 is a prerequisite for nuclear lamina assembly. J Cell Biol 150: 1251-1262.
130. Stegmeier F, Amon A. 2004. Closing mitosis: The functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38: 203-232.
131. Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW. 2001. Dual inhibition of sister chromatid separation at metaphase. Cell 107: 715-26.
132. Su TT, Sprenger F, DiGregorio PJ, Campbell SD, O’Farrell PH. 1998. Exit from mitosis in Drosophila syncytial embryos requires proteolysis and cyclin degradation, and is associated with localized dephosphorylation. Genes Dev 12: 1495-1503.
133. Sudakin V, Chan GK, Yen TJ. 2001. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 154: 925-936.
134. Sumara I, Quadroni M, Frei C, Olma MH, Sumara G, Ricci R, Peter M. 2007. ACul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev Cell 12: 887-900.
135. Takizawa CG, Weis K, Morgan DO. 1999. Ran-independent nuclear import of cyclin B1-Cdc2 by importin b. Proc Natl Acad Sci 96: 7938-7943.
136. Tang Z, Shu H, Qi W, Mahmood NA, Mumby MC, Yu H. 2006. PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev Cell 10: 575-585.
137. Teichner A, Eytan E, Sitry-Shevah D, Miniowitz-Shemtov S, Dumin E, Gromis J, Hershko A. 2011. p31comet promotes disassembly of the mitotic checkpoint complex in an ATP-dependent process. Proc Natl Acad Sci 108: 3187-3192.
138. Toyoshima F, Moriguchi T, Wada A, Fukuda M, Nishida E. 1998. Nuclear export of cyclin B1 and its possible role in the DNA damage-induced G2 checkpoint. EMBO J 17: 2728-2735.
139. Toyoshima-Morimoto F, Taniguchi E, Shinya N, Iwamatsu A, Nishida E. 2001. Polo-like kinase 1 phosphorylates cyclin B1 and targets it to the nucleus during prophase. Nature 410: 215-220.
140. Toyoshima-Morimoto F, Taniguchi E, Nishida E. 2002. Plk1 promotes nuclear translocation of human Cdc25C during prophase. EMBO Rep 3: 341-348.
141. Trunnell NB, Poon AC, Kim SY, Ferrell JEJ. 2011. Ultrasen-sitivity in the regulation of Cdc25C by Cdk1. Mol Cell 41: 263-274.
142. Uzunova K, Dye BT, Schutz H, Ladurner R, Petzold G, Toyoda Y, Jarvis MA, Brown NG, Poser I, Novatchkova M, et al. 2012. APC15 mediates CDC20 autoubiquityla-tionbyAPC/CMCCand disassemblyof the mitotic checkpoint complex. Nat Struct Mol Biol 19: 1116-1123.
143. Vagnarelli P, Ribeiro S, Sennels L, Sanchez-Pulido L, deLima Alves F, Verheyen T, Kelly DA, Ponting CP, Rappsilber J, Earnshaw WC. 2011. Repo-Man coordinates chromosomal reorganization with nuclear envelope reassembly during mitotic exit. Dev Cell 21: 328-342.
144. Virshup DM, Shenolikar S. 2009. From promiscuity to precision: Protein phosphatases get a makeover. Mol Cell 33: 537-545.
145. Wang K, Sturt-Gillespie B, Hittle JC, Macdonald D, Chan GK, Yen TJ, Liu S-T. 2014. Thyroid hormone receptor interacting protein 13 (TRIP13) AAA-ATPase is a novel mitotic checkpoint-silencing protein. J Biol Chem 289: 23928-23937.
146. Watanabe N, Broome M, Hunter T. 1995. Regulation of the human Wee1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J 14: 1878-1891.
147. Westhorpe FG, Straight AF. 2015. The centromere: Epige-netic control of chromosome segregation during mitosis. Cold Spring Harb Perspect Biol 7: a015818.
148. Westhorpe FG, Tighe A, Lara-Gonzalez P, Taylor SS. 2011. p31comet-mediated extraction of Mad2 from the MCC promotes efficient mitotic exit. J Cell Sci 124: 3905-3916.
149. Wilde A, Lizarraga SB, Zhang L, Wiese C, Gliksman NR, Walczak CE, Zheng Y. 2001. Ran stimulates spindle as-semblybyaltering microtubule dynamics and the balance of motor activities. Nat Cell Biol 3: 221-227.
150. Williams BC, Filter JJ, Blake-Hodek KA, Wadzinski BE, Fuda NJ, Shalloway D, Goldberg ML. 2014. Greatwall-phos-phorylated Endosulfine is both an inhibitor and a substrate of PP2A-B55 heterotrimers. Elife 3: e01695.
151. Williamson A, Banerjee S, Zhu X, Philipp I, Iavarone AT, Rape M.2011. Regulation of ubiquitin chain initiation to control the timing of substrate degradation. Mol Cell 42: 744-757.
152. Wittmann T, Wilm M, Karsenti E, Vernos I. 2000. TPX2, A novel Xenopus MAP involved in spindle pole organization. J Cell Biol 149: 1405-1418.
153. Wolthuis R, Clay-Farrace L, van Zon W, Yekezare M, Koop L, Ogink J, Medema R, Pines J. 2008. Cdc20 and Cks direct the spindle checkpoint-independent destruction of cy-clin A. Mol Cell 30: 290-302.
154. Wu JQ, Guo JY, Tang W, Yang C-S, Freel CD, Chen C, Nairn AC, Kornbluth S. 2009. PP1-mediated dephosphoryla-tion of phosphoproteins at mitotic exit is controlled by inhibitor-1 and PP1 phosphorylation. Nat Cell Biol 11: 644-651.
155. Wurzenberger C, Held M, Lampson MA, Poser I, Hyman AA, Gerlich DW. 2012. Sds22 and Repo-Man stabilize chromosome segregation by counteracting Aurora B on anaphase kinetochores. J Cell Biol 198: 173-183.
156. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G, et al. 1997. Sequence-specific and phosphorylation-de-pendent proline isomerization: A potential mitotic regulatory mechanism. Science 278: 1957-1960.
157. Yanagida M. 2014. The role of model organisms in the history of mitosis research. Cold Spring Harb Perspect Biol 6: a015768.
158. Yang J, Bardes ES, Moore JD, Brennan J, Powers MA, Korn-bluth S. 1998. Control of cyclin B1 localization through regulated binding of the nuclear export factor CRM1. Genes Dev 12: 2131-2143.
159. Yokoyama H, Gruss OJ, Rybina S, Caudron M, Schelder M, Wilm M, Mattaj IW, Karsenti E.2008.Cdk11isaRanGTP-dependent microtubule stabilization factor that regulates spindle assembly rate. J Cell Biol 180: 867-875.
160. Zeng K, Bastos RN, Barr FA, Gruneberg U. 2010. Protein phosphatase 6 regulates mitotic spindle formation by controlling the T-loop phosphorylation state of Aurora A bound to its activator TPX2. J Cell Biol 191: 1315-1332.