A quantitative model for cyclin-dependent kinase control of the cell cycle: Revisited

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1584, 2011, Pages 3572-3583

  Uhlmann, Frank ^a   Bouchoux, Céline ^a   López Avilés, Sandra ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Cell cycle; Cyclin dependent kinase (Cdk); Mitosis; Phosphatases; Quantitative biology; S phase

Indexed keywords

CHROMOSOME; ENZYME ACTIVITY; EUKARYOTE; EXPERIMENTAL STUDY; MOLECULAR ANALYSIS; NUMERICAL MODEL; QUANTITATIVE ANALYSIS; RECONSTRUCTION; YEAST;

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

EID: 81055137194     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0082     Document Type: Review

References (114)

1. van Werven, F. J. & Amon, A. 2011 Regulation of entry into gametogenesis. Phil. Trans. R. Soc. B. 366, 3521-3531. (doi:10.1098/rstb.2011.0081)
2. O'Farrell, P. H. 2011 Quiescence: early evolutionary origins and universality do not imply uniformity. Phil. Trans. R. Soc. B. 366, 3498-3507. (doi:10.1098/rstb. 2011.0079)
3. Kronja, I. & Orr-Weaver, T. L. 2011 Translational regulation of the cell cycle: when, where, how and why? Phil. Trans. R. Soc. B. 366, 3638-3652. (doi:10. 1098/rstb.2011.0084)
4. Ptacin, J. L., Lee, S. F., Garner, E. C., Toro, E., Eckart, M., Comolli, L. R., Moerner, W. E. & Shapiro, L. 2010 A spindle-like apparatus guides bacterial chromosome segregation. Nat. Cell Biol. 12, 791-798. (doi:10. 1038/ncb2083)
5. Nasmyth, K. 1995 Evolution of the cell cycle. Phil. Trans. R Soc. Lond. B 349, 271-281. (doi:10.1098/ rstb.1995.0113)
6. Stern, B. & Nurse, P. 1996 A quantitative model for the cdc2 control of S phase and mitosis in fission yeast. Trends Genet. 12, 345-350.
7. Nurse, P. & Bissett, Y. 1981 Gene requirement in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature 292, 558-560. (doi:10. 1038/292558a0)
8. Piggott, J. R., Rai, R. & Carter, B. L. A. 1982 A bifunctional gene product involved in two phases of the cell cycle. Nature 298, 391-393. (doi:10.1038/298391a0)
9. Hartwell, L. H. & Weinert, T. A. 1989 Checkpoints: controls that ensure the order of cell cycle events. Science 246, 629-634. (doi:10.1126/science.2683079)
10. Murray, A. W. & Kirschner, M. W. 1989 Dominoes and clocks: the union of two views of the cell cycle. Science 246, 614-621. (doi:10.1126/science.2683077)
11. Hayles, J., Fisher, D., Woollard, A. & Nurse, P. 1994 Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2-mitotic B cyclin complex. Cell 78, 813-822. (doi:10.1016/ S0092-8674(94)90542-8)
12. Nasmyth, K. 1995 How do cells control the timing of DNAreplication and mitosis? Harvey Lect. 88, 141-171.
13. Weinert, T. A. & Hartwell, L. H. 1988 The RAD9 gene controls the cell cycle response to DNA damagein Saccharomyces cerevisiae. Science 241, 317-322. (doi:10.1126/science.3291120)
14. Enoch, T. & Nurse, P. 1990 Mutation of fission yeast cell cycle control genes abolishes the dependence of mitosis on DNA replication. Cell 60, 665-673. (doi:10.1016/0092-8674(90)90669-6)
15. Minshull, J., Golsteyn, R., Hill, C. S. & Hunt, T. 1990 The A- and B-type cyclin associated cdc2 kinase in Xenopus turn on and off at different times in the cycle. EMBO J. 9, 2865-2875.
16. Surana, U., Robitsch, H., Price, C., Schuster, T., Fitch, I., Futcher, A. B. & Nasmyth, K. 1991 The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 65, 145-161. (doi:10.1016/0092-8674(91)90416-V)
17. Coudreuse, D. & Nurse, P. 2010 Driving the cell cycle with a minimal CDK control network. Nature 468, 1074-1079. (doi:10.1038/nature09543)
18. Rhind, N. 2006 DNA replication timing: random thoughts about origin firing. Nat. Cell Biol. 8, 1313-1316. (doi:10.1038/ncb1206-1313)
19. Gerhart, J., Wu, M. & Kirschner, M. 1984 Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J. Cell Biol. 98, 1247-1255. (doi:10.1083/jcb.98.4.1247)
20. Hartwell, L. H. 1978 Cell division from a genetic perspective. J. Cell Biol. 77, 627-637. (doi:10.1083/ jcb.77.3.627)
21. Michael, W. M., Ott, R., Fanning, E. & Newport, J. 2000 Activation of the DNA replication checkpoint through RNA synthesis by primase. Science 289, 2133-2137. (doi:10.1126/science.289.5487.2133)
22. Bartek, J., Lukas, C. & Lukas, J. 2004 Checking on DNA damage in S phase. Nat. Rev. Mol. Cell Biol. 5, 793-804. (doi:10.1038/nrm1493)
23. Lisby, M., Rothstein, R. & Mortensen, U. H. 2001 Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl Acad. Sci. USA 98, 8276- 8282. (doi:10.1073/pnas.121006298)
24. Lengronne, A. & Schwob, E. 2002 The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G1. Mol. Cell 9, 1067-1078. (doi:10.1016/S1097-2765(02)00513-0)
25. Santaguida, S. & Musacchio, A. 2009 The life and miracles of kinetochores. EMBO J. 28, 2511-2531. (doi:10.1038/emboj.2009.173)
26. Li, R. & Murray, A. W. 1991 Feedback control of mitosis in budding yeast. Cell 66, 519-531. (doi:10.1016/0092-8674(81)90015-5)
27. Hoyt, M. A., Totis, L. & Roberts, B. T. 1991 S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66, 507-517. (doi:10.1016/0092-8674(81)90014-3)
28. Liu, D., Vader, G., Vromans, M. J. M., Lampson, M. A. & Lens, S. M. A. 2009 Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353. (doi:10.1126/science.1167000)
29. Palframan, W. J., Meehl, J. B., Jaspersen, S. L., Winey, M. & Murray, A. W. 2006 Anaphase inactivation of the spindle checkpoint. Science 313, 680-684. (doi:10. 1126/science.1127205)
30. Mirchenko, L. & Uhlmann, F. 2010 Sli15 INCENP dephosphorylation prevents mitotic checkpoint reengagement due to loss of tension at anaphase onset. Curr. Biol. 20, 1396-1401. (doi:10.1016/j.cub.2010.06.023)
31. Dobles, M., Liberal, V., Scott, M. L., Benezra, R. & Sorger, P. K. 2000 Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101, 635-645. (doi:10.1016/S0092-8674(00)80875-2)
32. Nash, R., Tokiwa, G., Anand, S., Erickson, K. & Futcher, A. B. 1988 The WHI1{thorn} gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog. EMBO J. 7, 4335-4346.
33. Richardson, H. E.,Wittenberg, C., Cross, F. & Reed, S. I. 1989 An essential G1 function for cyclin-like proteins in yeast. Cell 59, 1127-1133. (doi:10.1016/0092-8674(89)90768-X)
34. Minshull, J., Blow, J. J. & Hunt, T. 1989 Translation of cyclin mRNA is necessary for extracts of activated Xenopus eggs to enter mitosis. Cell 56, 947-956. (doi:10. 1016/0092-8674(89)90628-4)
35. Ghiara, J. B., Richardson, H. E., Sugimoto, K., Henze, M., Lew, D. J., Wittenberg, C. & Reed, S. I. 1991 A cyclin B homolog in S. cerevisiae: chronic activation of the Cdc28 protein kinase by cyclin prevents exit from mitosis. Cell 65, 163-174. (doi:10.1016/0092-8674(91)90417-W)
36. Epstein, C. B. & Cross, F. 1992 CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 6, 1695-1706. (doi:10.1101/gad.6.9.1695)
37. Schwob, E. & Nasmyth, K. 1993 CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes. Dev. 7, 1160-1175. (doi:10.1101/gad.7.7a.1160)
38. Amon, A., Tyers, M., Futcher, B. & Nasmyth, K. 1993 Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74, 993-1007. (doi:10.1016/0092-8674(93)90722-3)
39. Kitagawa, M. et al. 1996 The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15, 7060-7069.
40. Russo, A. A., Jeffrey, P. D., Patten, A. K., Massague, J. & Pavletich, N. P. 1996 Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382, 325-331. (doi:10.1038/382325a0)
41. Brown, N. R., Noble, M. E. M., Endicott, J. A. & Johnson, L. N. 1999 The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat. Cell Biol. 1, 438-443. (doi:10.1038/15674)
42. Adams, P. D., Sellers, W. R., Sharma, S. K., Wu, A. D., Nalin, C. M. & Kaelin, J. W. G. 1996 Identification of a cyclin-cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol. Cell. Biol. 16, 6623-6633.
43. Petri, E. T., Errico, A., Escobedo, L., Hunt, T. & Basavappa, R. 2007 The crystal structure of human cyclin B. Cell Cycle 6, 1342-1349. (doi:10.4161/cc.6.11.4297)
44. Day, P. J. et al. 2009 Crystal structure of humanCDK4 in complex with a D-type cyclin. Proc. Natl Acad. Sci. USA 106, 4166-4170. (doi:10.1073/pnas.0809645106)
45. Takaki, T., Echalier, A., Brown, N. R., Hunt, T., Endicott, J. A. & Noble, M. E. M. 2009 The structure of CDK4/cyclin D3 has implications for models of CDK activation. Proc. Natl Acad. Sci. USA 106, 4171-4176. (doi:10.1073/pnas.0809674106)
46. Ubersax, J. A., Woodbury, E. L., Quang, P. N., Paraz, M., Blethrow, J. D., Shah, K., Shokat, K. M. & Morgan, D. O. 2003 Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864. (doi:10.1038/ nature02062)
47. Loog, M. & Morgan, D. O. 2005 Cyclin specificity in the phosphorylation of cyclin-dependent kinasesubstrates. Nature 434, 104-108. (doi:10.1038/ nature03329)
48. Tanaka, S., Umemori, T., Hirai, K., Muramatsu, S., Kamimura, Y. & Araki, H. 2007 CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445, 328-332. (doi:10.1038/ nature05465)
49. Zegerman, P. & Diffley, J. F. X. 2007 Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445, 281-285. (doi:10.1038/nature05432)
50. Cross, F. R., Yuste-Rojas, M., Gray, S. & Jacobson, M. D. 1999 Specialization and targeting of B-type cyclins. Mol. Cell 4, 11-19. (doi:10.1016/S1097-2765(00)80183-5)
51. Hu, F. & Aparicio, O. M. 2005 Swe1 regulation and transcriptional control restrict the activity of mitotic cyclins toward replication proteins in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 102, 8910-8915. (doi:10.1073/pnas.0406987102)
52. Moore, J. D., Kirk, J. A. & Hunt, T. 2003 Unmasking the S-phase-promoting potential of cyclin B1. Science 300, 987-990. (doi:10.1126/science.1081418)
53. Tyers, M. 1996 The cyclin-dependent kinase inhibitor p40SIC1 imposes the requirement for Cln G1 cyclin function at Start. Proc. Natl Acad. Sci. USA 93, 7772-7776. (doi:10.1073/pnas.93.15.7772)
54. Fitch, I. T., Dahmann, C., Surana, U., Amon, A., Nasmyth, K., Goetsch, L., Byers, B. & Futcher, B. 1992 Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell 3, 805-818.
55. Schwob, E., Böhm, T., Mendenhall, M. D. & Nasmyth, K. 1994 The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. Cerevisiae. Cell 79, 233-244. (doi:10.1016/0092-8674(94)90193-7)
56. Haase, S. B. & Reed, S. I. 1999 Evidence that a freerunning oscillator drives G1 events in the budding yeast cell cycle. Nature 401, 394-397. (doi:10.1038/43927)
57. Martin-Castallanos, C., Blanco, M. A., de Prada, J. M. & Moreno, S. 2000 The puc1 cyclin regulates the G1 phase of the fission yeast cell cycle in response to cell size. Mol. Biol. Cell 11, 543-554.
58. Hagan, I., Hayles, J. & Nurse, P. 1988 Cloning and sequencing of the cyclin-related cdc13{thorn} gene and a cytological study of its role in fission yeast mitosis. J. Cell Sci. 91, 587-595.
59. Kozar, K. et al. 2004 Mouse development and cell proliferation in the absence of D-cyclins. Cell 118, 477-491. (doi:10.1016/j.cell.2004.07.025)
60. Geng, Y. et al. 2003 Cyclin E ablation in the mouse. Cell 114, 431-443. (doi:10.1016/S0092-8674(03)00645-7)
61. Liu, D., Matzuk, M. M., Sung, W. K., Guo, Q., Wang, P. & Wolgemuth, D. J. 1998 Cyclin A1 is required for meiosis in the male mouse. Nat. Genet. 20, 377-380. (doi:10.1038/3855)
62. Murphy, M., Stinnakre, M.-G., Senamaud-Beaufort, C., Winston, N. J., Sweeney, C., Kubelka, M., Carrington, M., Brechot, C. & Sobczak-Thépot, J. 1997 Delayed early embryonic lethality following disruption of the murine cyclin A2 gene. Nat. Genet. 15, 83-86. (doi:10. 1038/ng0197-83)
63. Kalaszczynska, I. et al. 2009 Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells. Cell 138, 352-565. (doi:10. 1016/j.cell.2009.04.062)
64. Brandeis, M., Rosewell, I., Carrington, M., Crompton, T., Jacobs, M. A., Kirk, J., Gannon, J. & Hunt, T. 1998 Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc. Natl Acad. Sci. USA 95, 4344-4349. (doi:10. 1073/pnas.95.8.4344)
65. Hochegger, H., Takeda, S. & Hunt, T. 2008 Cyclindependent kinases and cell-cycle transitions: does one fit all? Nat. Rev. Mol. Cell Biol. 9, 910-916. (doi:10. 1038/nrm2510)
66. Lopez-Girona, A., Mondesert, O., Leatherwood, J. & Russell, P. 1998 Negative regulation of Cdc18 DNA replication protein by Cdc2. Mol. Biol. Cell 9, 63-73.
67. Merrick, K. A., Larochelle, S., Zhang, C., Allen, J. J., Shokat, K. M. & Fisher, R. P. 2008 Distinct activation pathways confer cyclin-binding specificity on Cdk1 and Cdk2 in human cells. Mol. Cell 32, 662-672. (doi:10.1016/j.molcel.2008.10.022)
68. Santamaria, D. et al. 2007 Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448, 811-815. (doi:10.1038/nature06046)
69. Booher, R. & Beach, D. 1988 Involvement of cdc13{thorn} in mitosis control in Schizosaccharomyces pombe: possible interaction of the gene product with microtubules. EMBO J. 7, 2321-2327.
70. Forsburg, S. L. & Nurse, P. 1991 Identification of a G1- type cyclin puc1{thorn} in the fission yeast Schizosaccharomyces pombe. Nature 351, 245-248. (doi:10.1038/351245a0)
71. Bueno, A., Richardson, H., Reed, S. I. & Russell, P. 1991 A fission yeast B-type cyclin functioning early in the cell cycle. Cell 66, 149-159. (doi:10.1016/0092-8674(91)90147-Q)
72. Bueno, A. & Russell, P. 1993 Two fission yeast B-type cyclins, Cig2 and Cdc13, have different functions in mitosis. Mol. Cell. Biol. 13, 2286-2297.
73. Connolly, T. & Beach, D. 1994 Interaction between the Cig1 and Cig2 B-type cyclins in the fission yeast cell cycle. Mol. Cell. Biol. 14, 768-776.
74. Obara-Ishihara, T. & Okayama, H. 1994 A B-type cyclin negatively regulates conjugation via interacting with cell cycle 'start' genes in fission yeast. EMBO J. 13, 1863-1872.
75. Fisher, D. L. & Nurse, P. 1996 A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins. EMBO J. 15, 850-860.
76. Moreno, S. & Nurse, P. 1994 Regulation of progression through the G1 phase of the cell cycle by the rum1{thorn} gene. Nature 367, 236-242. (doi:10.1038/367236a0)
77. Stern, B. & Nurse, P. 1998 Cyclin B proteolysis and the cyclin-dependent kinase inhibitor rum1p are required for pheromone-induced G1 arrest in fission yeast. Mol. Biol. Cell 9, 1309-1321.
78. Russell, P. & Nurse, P. 1987 Negative regulation of mitosis by wee1{thorn}, a gene encoding a protein kinase homolog. Cell 49, 559-567. (doi:10.1016/0092-8674(87)90458-2)
79. Gould, K. L. & Nurse, P. 1989 Tyrosine phosphorylation of the fission yeast cdc2{thorn} protein kinase regulates entry into mitosis. Nature 342, 39-45. (doi:10.1038/342039a0)
80. Dunphy, W. G. & Newport, J. W. 1989 Fission yeast p13 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc2 protein kinase. Cell 58, 181-191. (doi:10.1016/0092-8674(89)90414-5)
81. Morla, A. O., Draetta, G., Beach, D. & Wang, J. Y. J. 1989 Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis. Cell 58, 193-203. (doi:10.1016/0092-8674(89)90415-7)
82. Ghaemmaghami, S., Huh, W.-K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K. & Weissman, J. S. 2003 Global analysis of proteinexpression in yeast. Nature 425, 737-741. (doi:10.1038/nature02046)
83. Glotzer, M., Murray, A. W. & Kirschner, M. W. 1991 Cyclin is degraded by the uniquitin pathway. Nature 349, 132-138. (doi:10.1038/349132a0)
84. Wolf, F., Wandke, C., Isenberg, N. & Geley, S. 2006 Dose-dependent effects of stable cyclin B1 on progression through mitosis in human cells. EMBO J. 25, 2802-2813. (doi:10.1038/sj.emboj.7601163)
85. Drapkin, B. J., Lu, Y., Procko, A. L., Timney, B. L. & Cross, F. R. 2009 Analysis of the mitotic exit control system using locked levels of stable mitotic cyclin. Mol. Syst. Biol. 5, 328. (doi:10.1038/msb.2009.78)
86. Visintin, R., Craig, K., Hwang, E. S., Prinz, S., Tyers, M. & Amon, A. 1998 The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2, 709-718. (doi:10.1016/ S1097-2765(00)80286-5)
87. Pereira, G. & Schiebel, E. 2003 Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 302, 2120-2124. (doi:10.1126/science.1091936)
88. Higuchi, T. & Uhlmann, F. 2005 Stabilization of microtubule dynamics at anaphase onset promotes chromosome segregation. Nature 433, 171-176. (doi:10.1038/nature03240)
89. Zhu, C., Lau, E., Schwarzenbacher, R., Bossy-Wetzel, E. & Jiang, W. 2006 Spatiotemporal control of spindle midzone formation by PRC1 in human cells. Proc. Natl Acad. Sci. USA 103, 6196-6201. (doi:10.1073/ pnas.0506926103)
90. Woodbury, E. L. & Morgan, D. O. 2007 Cdk and APC activities limit the spindle-stabilizing function of Fin1 to anaphase. Nat. Cell Biol. 9, 106-112. (doi:10.1038/ ncb1523)
91. Khmelinskii, A., Roostalu, J., Roque, H., Antony, C. & Schiebel, E. 2009 Phosphorylation-dependent protein interactions at the spindle midzone mediate cell cycle regulation of spindle elongation. Dev. Cell 17, 244-256. (doi:10.1016/j.devcel.2009.06.011)
92. Stegmeier, F. & Amon, A. 2004 Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38, 203-231. (doi:10.1146/annurev. genet.38.072902.093051)
93. Queralt, E. & Uhlmann, F. 2008 Cdk-counteracting phosphatases unlock mitotic exit. Curr. Opin. Cell Biol. 20, 661-668. (doi:10.1016/j.ceb.2008.09.003)
94. Jin, F., Liu, H., Liang, F., Rizkallah, R., Hurt, M. M. & Wang, Y. 2008 Temporal control of the dephosphorylation of Cdk substrates by mitotic exit pathways in budding yeast. Proc. Natl Acad. Sci. USA 105, 16 177-16 182. (doi:10.1073/pnas.0808719105)
95. 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, 207-220. (doi:10.1016/S0092-8674(02)00618-9)
96. Azzam, R., Chen, S. L., Shou, W., Mah, A. S., Alexandru, G., Nasmyth, K., Annan, R. S., Carr, S. A. & Deshaies, R. J. 2004 Phosphorylation by cyclin B-Cdk underlies release of mitotic exit activator Cdc14 from the nucleolus. Science 305, 516-519. (doi:10.1126/science.1099402)
97. Queralt, E., Lehane, C., Novak, B. & Uhlmann, F. 2006 Downregulation of PP2ACdc55 phosphatase by separase initiates mitotic exit in budding yeast. Cell 125, 719-732. (doi:10.1016/j.cell.2006.03.038)
98. Liakopoulos, D., Kusch, J., Grava, S., Vogel, J. & Barral, Y. 2003 Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell 112, 561-574. (doi:10.1016/S0092-8674(03)00119-3)
99. Mochida, S., Ikeo, S., Gannon, J. & Hunt, T. 2009 Regulated activity of PP2A-B55d is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 28, 2777-2785. (doi:10.1038/ emboj.2009.238)
100. Wolfe, B. A., McDonald, W. H., Yates III J. R. & Gould, K. L. 2006 Phospho-regulation of the Cdc14/ Clp1 phosphatase delays late mitotic events in S. pombe. Dev. Cell 11, 423-430. (doi:10.1016/j.devcel.2006.07.016)
101. Bouchoux, C. & Uhlmann, F. In press. A quantitative model for ordered Cdk substrate dephosphorylation during mitotic exit. Cell (doi:10.1016/j.cell.2011.09.047)
102. Kinoshita, N., Yamano, H., Niwa, H., Yoshida, T. & Yanagida, M. 1993 Negative regulation of mitosis by the fission yeast protein phosphatase ppa2. Genes Dev. 7, 1059-1071. (doi:10.1101/gad.7.6.1059)
103. Wolfe, B. A. & Gould, K. L. 2004 Fission yeast Clp1p phosphatase affects G2/M transition and mitotic exit through Cdc25p inactivation. EMBO J. 23, 919-929. (doi:10.1038/sj.emboj.7600103)
104. Lee, T. H., Turck, C. & Kirschner, M. W. 1994 Inhibition of cdc2 activation by INH/PP2A. Mol. Biol. Cell 5, 323-338.
105. Novak, B. & Tyson, J. J. 1993 Numerical analysis of a comprehensive model of M-phase control in Xenopus oocyte extracts and intact embryos. J. Cell Sci. 106, 1153-1168.
106. Tyers, M. & Cook, M. 2007 Size control goes global. Curr. Opin. Biotechnol. 18, 341-350. (doi:10.1016/j. copbio.2007.07.006)
107. Nurse, P. 2011 Obituary: Murdoch Mitchison 1922-2011. Nat. Cell Biol. 13, 520. (doi:10.1038/ncb0511-520)
108. Nurse, P. 1975 Genetic control of cell size at cell division in yeast. Nature 256, 547-551. (doi:10.1038/256547a0)
109. Martin, S. G. & Berthelot-Grosjean, M. 2009 Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 459, 852-856. (doi:10.1038/nature08054)
110. Moseley, J. B., Mayeux, A., Paoletti, A. & Nurse, P. 2009 A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 459, 857-860. (doi:10.1038/nature08074)
111. Jorgensen, P., Nishikawa, J. L., Breitkreutz, B.-J. & Tyers, M. 2002 Systematic identification of pathways that couple cell growth and division in yeast. Science 297, 395-400. (doi:10.1126/science.1070850)
112. Zhurinsky, J., Leonhard, K., Watt, S., Marguerat, S., B ä hler, J. & Nurse, P. 2010 A coordinated global control over cellular transcription. Curr. Biol. 20, 2010-2015. (doi:10.1016/j.cub.2010.10.002)
113. Tokiwa, G., Tyers, M., Vople, T. & Futcher, B. 1994 Inhibition of G1 cyclin activity by the Ras/cAMP pathway in yeast. Nature 371, 342-345. (doi:10.1038/371342a0)
114. Wang, H., Carey, L. B., Cai, Y., Wijnen, H. & Futcher, B. 2009 Recruitment of Cln3 cyclin to promoters controls cell cycle entry via histone deacetylase and other targets. PLoS Biol. 7, e1000189. (doi:10.1371/journal. pbio.1000189)