A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes

Development

Volumn 138, Issue 17, 2011, Pages 3735-3744

  Gaffré, Melina ^a,b   Martoriati, Alain ^a,b   Belhachemi, Naima ^a,b   Chambon, Jean Philippe ^a,b   Houliston, Evelyn ^a,b   Jessus, Catherine ^a,b   Karaiskou, Anthi ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

Author keywords

Cdc2; Cyclin B; Meiosis; Myt1; Oocyte; Xenopus

Indexed keywords

CELL PROTEIN; CYCLIN B; CYCLIN DEPENDENT KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PROGESTERONE; PROTEIN MYT1; PROTEIN PLX; PROTEIN TYROSINE PHOSPHATASE; THREONINE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE ARREST; CELL CYCLE M PHASE; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; FEMALE; GENE AMPLIFICATION; MEIOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROPHASE; PROTEIN SYNTHESIS; UPREGULATION; XENOPUS;

ANIMALS; BLOTTING, WESTERN; CYCLIN B; MEIOSIS; MODELS, BIOLOGICAL; OOCYTES; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; XENOPUS; XENOPUS PROTEINS;

EID: 80051523977     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.063974     Document Type: Article

References (54)

1. Abrieu, A., Brassac, T., Galas, S., Fisher, D., Labbe, J. C. and Doree, M. (1998). The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs. J. Cell Sci. 111, 1751-1757.
2. Amiel, A., Leclere, L., Robert, L., Chevalier, S. and Houliston, E. (2009). Conserved functions for Mos in eumetazoan oocyte maturation revealed by studies in a cnidarian. Curr. Biol. 19, 305-311.
3. Booher, R. N., Holman, P. S. and Fattaey, A. (1997). Human Myt1 is a cell cycleregulated kinase that inhibits Cdc2 but not Cdk2 activity. J. Biol. Chem. 272, 22300-22306.
4. Burrows, A. E., Sceurman, B. K., Kosinski, M. E., Richie, C. T., Sadler, P. L., Schumacher, J. M. and Golden, A. (2006). The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133, 697-709.
5. Coleman, T. R. and Dunphy, W. G. (1994). Cdc2 regulatory factors. Curr. Opin. Cell Biol. 6, 877-882.
6. De Smedt, V., Rime, H., Jessus, C. and Ozon, R. (1995). Inhibition of glycosphingolipid synthesis induces p34cdc2 activation in Xenopus oocyte. FEBS Lett. 375, 249-253.
7. Deibler, R. W. and Kirschner, M. W. (2010). Quantitative reconstitution of mitotic CDK1 activation in somatic cell extracts. Mol. Cell 37, 753-767.
8. Descombes, P. and Nigg, A. E. (1998). The polo-like kinase Plx1 is required for M phase exit and destruction of mitotic regulators in Xenopus egg extracts. EMBO J. 17, 1328-1335.
9. Dupre, A., Jessus, C., Ozon, R. and Haccard, O. (2002). Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. EMBO J. 21, 4026-4036.
10. Elia, A. E., Rellos, P., Haire, L. F., Chao, J. W., Ivins, F. J., Hoepker, K., Mohammad, D., Cantley, L. C., Smerdon, S. J. and Yaffe, M. B. (2003). The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115, 83-95.
11. Ferby, I., Blazquez, M., Palmer, A., Eritja, R. and Nebreda, A. R. (1999). A novel p34(cdc2)-binding and activating protein that is necessary and sufficient to trigger G(2)/M progression in Xenopus oocytes. Genes Dev. 13, 2177-2189.
12. Fisher, D. L., Brassac, T., Galas, S. and Doree, M. (1999). Dissociation of MAP kinase activation and MPF activation in hormone-stimulated maturation of Xenopus oocytes. Development 126, 4537-4546.
13. Frank-Vaillant, M., Jessus, C., Ozon, R., Maller, J. L. and Haccard, O. (1999). Two distinct mechanisms control the accumulation of cyclin B1 and Mos in Xenopus oocytes in response to progesterone. Mol. Biol. Cell 10, 3279-3288.
14. Fung, T. K., Ma, H. T. and Poon, R. Y. (2007). Specialized roles of the two mitotic cyclins in somatic cells: cyclin A as an activator of M phase-promoting factor. Mol. Biol. Cell 18, 1861-1873.
15. Gross, S. D., Schwab, M. S., Taieb, F. E., Lewellyn, A. L., Qian, Y. W. and Maller, J. L. (2000). The critical role of the MAP kinase pathway in meiosis II in Xenopus oocytes is mediated by p90(Rsk). Curr. Biol. 10, 430-438.
16. Gutierrez, G. J., Vogtlin, A., Castro, A., Ferby, I., Salvagiotto, G., Ronai, Z., Lorca, T. and Nebreda, A. R. (2006). Meiotic regulation of the CDK activator RINGO/Speedy by ubiquitin-proteasome-mediated processing and degradation. Nat. Cell Biol. 8, 1084-1094.
17. Haccard, O. and Jessus, C. (2006). Redundant pathways for Cdc2 activation in Xenopus oocyte: either cyclin B or Mos synthesis. EMBO Rep. 7, 321-325.
18. Han, S. J., Chen, R., Paronetto, M. P. and Conti, M. (2005). Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr. Biol. 15, 1670-1676.
19. Hashimoto, O., Shinkawa, M., Torimura, T., Nakamura, T., Selvendiran, K., Sakamoto, M., Koga, H., Ueno, T. and Sata, M. (2006). Cell cycle regulation by the Wee1 inhibitor PD0166285, pyrido [2,3-d] pyimidine, in the B16 mouse melanoma cell line. BMC Cancer 6, 292.
20. Hochegger, H., Klotzbucher, A., Kirk, J., Howell, M., le Guellec, K., Fletcher, K., Duncan, T., Sohail, M. and Hunt, T. (2001). New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation. Development 128, 3795-3807.
21. Inoue, D. and Sagata, N. (2005). The Polo-like kinase Plx1 interacts with and inhibits Myt1 after fertilization of Xenopus eggs. EMBO J. 24, 1057-1067.
22. Izumi, T., Walker, D. H. and Maller, J. L. (1992). Periodic changes in phosphorylation of the Xenopus Cdc25 phosphatase regulate its activity. Mol. Biol Cell 3, 927-939.
23. Jessus, C., Ducommun, B. and Beach, D. (1990). Direct activation of cdc2 with phosphatase: identification of p13suc1-sensitive and insensitive steps. FEBS Lett. 266, 4-8.
24. Jessus, C., Rime, H., Haccard, O., Van, L. J., Goris, J., Merlevede, W. and Ozon, R. (1991). Tyrosine phosphorylation of p34cdc2 and p42 during meiotic maturation of Xenopus oocyte. Antagonistic action of okadaic acid and 6-DMAP. Development 111, 813-820.
25. Jin, Z., Homola, E. M., Goldbach, P., Choi, Y., Brill, J. A. and Campbell, S. D. (2005). Drosophila Myt1 is a Cdk1 inhibitory kinase that regulates multiple aspects of cell cycle behavior during gametogenesis. Development 132, 4075-4085.
26. Karaiskou, A., Cayla, X., Haccard, O., Jessus, C. and Ozon, R. (1998). MPF amplification in Xenopus oocyte extracts depends on a two-step activation of cdc25 phosphatase. Exp. Cell Res. 244, 491-500.
27. Karaiskou, A., Jessus, C., Brassac, T. and Ozon, R. (1999). Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF autoamplification. J. Cell Sci. 112, 3747-3756.
28. Karaiskou, A., Dupre, A., Haccard, O. and Jessus, C. (2001). From progesterone to active Cdc2 in Xenopus oocytes: a puzzling signalling pathway. Biol. Cell 93, 35-46.
29. Karaiskou, A., Lepretre, A. C., Pahlavan, G., Du Pasquier, D., Ozon, R. and Jessus, C. (2004). Polo-like kinase confers MPF autoamplification competence to growing Xenopus oocytes. Development 131, 1543-1552.
30. Kobayashi, H., Minshull, J., Ford, C., Golsteyn, R., Poon, R. and Hunt, T. (1991). On the synthesis and destruction of A- and B-type cyclins during oogenesis and meiotic maturation in Xenopus laevis. J. Cell Biol. 114, 755-765.
31. Kumagai, A., Yakowec, P. S. and Dunphy, W. G. (1998). 14-3-3 proteins act as negative regulators of the mitotic inducer Cdc25 in Xenopus egg extracts. Mol. Biol. Cell 9, 345-354.
32. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
33. Liu, F., Stanton, J. J., Wu, Z. Q. and PiwnicaWorms, 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.
34. Lorca, T., Bernis, C., Vigneron, S., Burgess, A., Brioudes, E., Labbe, J. C. and Castro, A. (2010). Constant regulation of both the MPF amplification loop and the Greatwall-PP2A pathway is required for metaphase II arrest and correct entry into the first embryonic cell cycle. J. Cell Sci. 123, 2281-2291.
35. Masui, Y. and Markert, C. L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129-146.
36. Morgan, D. O. (1995). Principles of CDK regulation. Nature 374, 131-134.
37. Mueller, P. R., Coleman, T. R., Kumagai, A. and Dunphy, W. G. (1995). Myt1: a membrane-associated inhibitory kinase that phosphorylates cdc2 on both threonine-14 and tyrosine-15. Science 270, 86-90.
38. Murakami, M. S. and Vande Woude, G. F. (1998). Analysis of the early embryonic cell cycles of Xenopus; regulation of cell cycle length by Xe-wee1 and Mos. Development 125, 237-248.
39. Nakajo, N., Yoshitome, S., Iwashita, J., Iida, M., Uto, K., Ueno, S., Okamoto, K. and Sagata, N. (2000). Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. Genes Dev. 14, 328-338.
40. Oh, J. S., Han, S. J. and Conti, M. (2010). Wee1B, Myt1, and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic resumption. J. Cell Biol. 188, 199-207.
41. Okamoto, K., Nakajo, N. and Sagata, N. (2002). The existence of two distinct Wee1 isoforms in Xenopus: implications for the developmental regulation of the cell cycle. EMBO J. 21, 2472-2484.
42. Okumura, E., Fukuhara, T., Yoshida, H., Hanada Si, S., Kozutsumi, R., Mori, M., Tachibana, K. and Kishimoto, T. (2002). Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat. Cell Biol. 4, 111-116.
43. Palmer, A., Gavin, A. C. and Nebreda, A. R. (1998). A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. EMBO J. 17, 5037-5047.
44. Panek, R. L., Lu, G. H., Klutchko, S. R., Batley, B. L., Dahring, T. K., Hamby, J. M., Hallak, H., Doherty, A. M. and Keiser, J. A. (1997). In vitro pharmacological characterization of PD 166285, a new nanomolar potent and broadly active protein tyrosine kinase inhibitor. J. Pharmacol. Exp. Ther. 283, 1433-1444.
45. Perry, J. A. and Kornbluth, S. (2007). Cdc25 and Wee1: analogous opposites? Cell Div. 2, 12.
46. Peter, M., Labbe, J. C., Doree, M. and Mandart, E. (2002). A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. Development 129, 2129-2139.
47. Pickham, K. M., Meyer, A. N., Li, J. K. and Donoghue, D. J. (1992). Requirement of mosxe protein kinase for meiotic maturation of Xenopus oocytes induced by a cdc2 mutant lacking regulatory phosphorylation sites. Mol. Cell. Biol. 12, 3192-3202.
48. 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.
49. Qian, Y. W., Erikson, E. and Maller, J. L. (1999). Mitotic effects of a constitutively active mutant of the Xenopus polo-like kinase Plx1. Mol. Cell. Biol. 19, 8625-8632.
50. Rime, H., Huchon, D., De Smedt, V., Thibier, C., Galaktionov, K., Jessus, C. and Ozon, R. (1994). Microinjection of Cdc25 protein phosphatase into Xenopus prophase oocyte activates MPF and arrests meiosis at metaphase I. Biol. Cell 82, 11-22.
51. Ruiz, E. J., Hunt, T. and Nebreda, A. R. (2008). Meiotic inactivation of Xenopus Myt1 by CDK/XRINGO, but not CDK/cyclin, via site-specific phosphorylation. Mol. Cell 32, 210-220.
52. Ruiz, E. J., Vilar, M. and Nebreda, A. R. (2010). A two-step inactivation mechanism of Myt1 ensures CDK1/Cyclin B activation and meiosis I entry. Curr. Biol. 20, 717-723.
53. Steegmaier, M., Hoffmann, M., Baum, A., Lenart, P., Petronczki, M., Krssak, M., Gurtler, U., Garin-Chesa, P., Lieb, S., Quant, J. et al. (2007). BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Curr. Biol. 17, 316-322.
54. Thibier, C., De Smedt, V., Poulhe, R., Huchon, D., Jessus, C. and Ozon, R. (1997). In vivo regulation of cytostatic activity in Xenopus metaphase II-arrested oocytes. Dev. Biol. 185, 55-66.