Robust mitotic entry is ensured by a latching switch

Biology Open

Volumn 2, Issue 9, 2013, Pages 924-931

  Tuck, Chloe ^a   Zhang, Tongli ^a   Potapova, Tamara ^b   Malumbres, Marcos ^c   Novák, Béla ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c Structural Biology and Biocomputing Programme   (Spain)

Author keywords

Cell cycle; G2 M transition; Greatwall kinase; Mitotic collapse; Mitotic entry; Spatial control of mitosis

Indexed keywords

EID: 84979246407     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20135199     Document Type: Article

References (45)

1. Arooz, T., Yam, C. H., Siu, W. Y., Lau, A., Li, K. K. and Poon, R. Y. (2000). On the concentrations of cyclins and cyclin-dependent kinases in extracts of cultured human cells. Biochemistry 39, 9494-9501.
2. Blake-Hodek, K. A., Williams, B. C., Zhao, Y., Castilho, P. V., Chen, W., Mao, Y., Yamamoto, T. M. and Goldberg, M. L. (2012). Determinants for activation of the atypical AGC kinase Greatwall during M phase entry. Mol. Cell. Biol. 32, 1337-1353.
3. Booher, R. N., Holman, P. S. and Fattaey, A. (1997). Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J. Biol. Chem. 272, 22300-22306.
4. Brizuela, L., Draetta, G. and Beach, D. (1989). Activation of human CDC2 protein as a histone H1 kinase is associated with complex formation with the p62 subunit. Proc. Natl. Acad. Sci. USA 86, 4362-4366.
5. Burgess, A., Vigneron, S., Brioudes, E., Labbé, J.-C., Lorca, T. and Castro, A. (2010). Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc. Natl. Acad. Sci. USA 107, 12564-12569.
6. Charvin, G., Oikonomou, C., Siggia, E. D. and Cross, F. R. (2010). Origin of irreversibility of cell cycle start in budding yeast. PLoS Biol. 8, e1000284.
7. Clarke, P. R., Hoffmann, I., Draetta, G. and Karsenti, E. (1993). Dephosphorylation of cdc25-C by a type-2A protein phosphatase: specific regulation during the cell cycle in Xenopus egg extracts. Mol. Biol. Cell 4, 397-411.
8. Cross, F. R., Archambault, V., Miller, M. and Klovstad, M. (2002). Testing a mathematical model of the yeast cell cycle. Mol. Biol. Cell 13, 52-70.
9. Dalal, S. N., Schweitzer, C. M., Gan, J. and DeCaprio, J. A. (1999). Cytoplasmic localization of human cdc25C during interphase requires an intact 14-3-3 binding site. Mol. Cell. Biol. 19, 4465-4479.
10. Domingo-Sananes, M. R., Kapuy, O., Hunt, T. and Novak, B. (2011). Switches and latches: a biochemical tug-of-war between the kinases and phosphatases that control mitosis. Philos. Trans. R. Soc. B 366, 3584-3594.
11. Draetta, G., Piwnica-Worms, H., Morrison, D., Druker, B., Roberts, T. and Beach, D. (1988). Human cdc2 protein kinase is a major cell-cycle regulated tyrosine kinase substrate. Nature 336, 738-744.
12. Drummond-Barbosa, D. and Spradling, A. C. (2004). α-endosulfine, a potential regulator of insulin secretion, is required for adult tissue growth control in Drosophila. Dev. Biol. 266, 310-321.
13. Galaktionov, K. and Beach, D. (1991). Specific activation of cdc25 tyrosine phosphatases by B-type cyclins: evidence for multiple roles of mitotic cyclins. Cell 67, 1181-1194.
14. Gavet, O. and Pines, J. (2010). Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J. Cell Biol. 189, 247-259.
15. Gharbi-Ayachi, A., Labbé, J.-C., Burgess, A., Vigneron, S., Strub, J.-M., Brioudes, E., Van-Dorsselaer, A., Castro, A. and Lorca, T. (2010). The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science 330, 1673-1677.
16. Hara, M., Abe, Y., Tanaka, T., Yamamoto, T., Okumura, E. and Kishimoto, T. (2012). Greatwall kinase and cyclin B-Cdk1 are both critical constituents of M-phase-promoting factor. Nat. Commun. 3, 1059.
17. He, E., Kapuy, O., Oliveira, R. A., Uhlmann, F., Tyson, J. J. and Novák, B. (2011). System-level feedbacks make the anaphase switch irreversible. Proc. Natl. Acad. Sci. USA 108, 10016-10021.
18. Heald, R., McLoughlin, M. and McKeon, F. (1993). Human wee1 maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase. Cell 74, 463-474.
19. Hoffmann, I., Clarke, P. R., Marcote, M. J., Karsenti, E. and Draetta, G. (1993). Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J. 12, 53-63.
20. Holt, L. J., Krutchinsky, A. N. and Morgan, D. O. (2008). Positive feedback sharpens the anaphase switch. Nature 454, 353-357.
21. Huber, M. D. and Gerace, L. (2007). The size-wise nucleus: nuclear volume control in eukaryotes. J. Cell Biol. 179, 583-584.
22. Joerger, A. C. and Fersht, A. R. (2007). Structure-function-rescue: the diverse nature of common p53 cancer mutants. Oncogene 26, 2226-2242.
23. Källström, H., Lindqvist, A., Pospisil, V., Lundgren, A. and Rosenthal, C. K. (2005). Cdc25A localisation and shuttling: characterisation of sequences mediating nuclear export and import. Exp. Cell Res. 303, 89-100.
24. Kim, M.-Y., Bucciarelli, E., Morton, D. G., Williams, B. C., Blake-Hodek, K., Pellacani, C., Von Stetina, J. R., Hu, X., Somma, M. P., Drummond-Barbosa, D. et al. (2012). Bypassing the Greatwall-Endosulfine pathway: plasticity of a pivotal cell-cycle regulatory module in Drosophila melanogaster and Caenorhabditis elegans. Genetics 191, 1181-1197.
25. Krek, W. and Nigg, E. A. (1991). Mutations of p34cdc2 phosphorylation sites induce premature mitotic events in HeLa cells: evidence for a double block to p34cdc2 kinase activation in vertebrates. EMBO J. 10, 3331-3341.
26. Liu, F., Stanton, J. J., Wu, Z. and Piwnica-Worms, H. (1997). The human Myt1 kinase preferentially phosphorylates Cdc2 on threonine 14 and localizes to the endoplasmic reticulum and Golgi complex. Mol. Cell. Biol. 17, 571-583.
27. López-Avilés, S., Kapuy, O., Novák, B. and Uhlmann, F. (2009). Irreversibility of mitotic exit is the consequence of systems-level feedback. Nature 459, 592-595.
28. McGowan, C. H. and Russell, P. (1993). Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. EMBO J. 12, 75-85.
29. Mochida, S., Ikeo, S., Gannon, J. and Hunt, T. (2009). Regulated activity of PP2A-B55 delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 28, 2777-2785.
30. Mochida, S., Maslen, S. L., Skehel, M. and Hunt, T. (2010). Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science 330, 1670-1673.
31. Morgan, D. (2006). The Cell Cycle: Principles Of Control. London: New Science Press.
32. Novak, B. and 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.
33. Novak, B., Tyson, J. J., Gyorffy, B. and Csikasz-Nagy, A. (2007). Irreversible cell-cycle transitions are due to systems-level feedback. Nat. Cell Biol. 9, 724-728.
34. Parker, L. L., Sylvestre, P. J., Byrnes, M. J., 3rd, Liu, F. and Piwnica-Worms, H. (1995). Identification of a 95-kDa WEE1-like tyrosine kinase in HeLa cells. Proc. Natl. Acad. Sci. USA 92, 9638-9642.
35. Pomerening, J. R., Sontag, E. D. and Ferrell, J. E., Jr. (2003). Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat. Cell Biol. 5, 346-351.
36. Pomerening, J. R., Ubersax, J. A. and Ferrell, J. E., Jr. (2008). Rapid cycling and precocious termination of G1 phase in cells expressing CDK1AF. Mol. Biol. Cell 19, 3426-3441.
37. Potapova, T. A., Sivakumar, S., Flynn, J. N., Li, R. and Gorbsky, G. J. (2011). Mitotic progression becomes irreversible in prometaphase and collapses when Wee1 and Cdc25 are inhibited. Mol. Biol. Cell 22, 1191-1206.
38. Santos, S. D. M., Wollman, R., Meyer, T. and Ferrell, J. E., Jr. (2012). Spatial positive feedback at the onset of mitosis. Cell 149, 1500-1513.
39. Sha, W., Moore, J., Chen, K., Lassaletta, A. D., Yi, C.-S., Tyson, J. J. and Sible, J. C. (2003). Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc. Natl. Acad. Sci. USA 100, 975-980.
40. Sveiczer, A., Novak, B. and Mitchison, J. M. (1996). The size control of fission yeast revisited. J. Cell Sci. 109, 2947-2957.
41. Sveiczer, A., Novak, B. and Mitchison, J. M. (1999). Mitotic control in the absence of cdc25 mitotic inducer in fission yeast. J. Cell Sci. 112, 1085-1092.
42. Verdugo, A., Vinod, P. K., Tyson, J. J. and Novak, B. (2013). Molecular mechanisms creating bistable switches at cell cycle transitions. Open Biology 3, 120179.
43. Voets, E. and Wolthuis, R. M. F. (2010). MASTL is the human orthologue of Greatwall kinase that facilitates mitotic entry, anaphase and cytokinesis. Cell Cycle 9, 3591-3601.
44. Watanabe, N., Broome, M. and Hunter, T. (1995). Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J. 14, 1878-1891.
45. Yu, J., Zhao, Y., Li, Z., Galas, S. and Goldberg, M. L. (2006). Greatwall kinase participates in the Cdc2 autoregulatory loop in Xenopus egg extracts. Mol. Cell 22, 83-91.