14-3-3 epsilon prevents G2/M transition of fertilized mouse eggs by binding with CDC25B
Tóm tắt
The 14-3-3 (YWHA) proteins are highly conserved in higher eukaryotes, participate in various cellular signaling pathways including cell cycle regulation, development and growth. Our previous studies demonstrated that 14-3-3ε (YWHAE) is responsible for maintaining prophase | arrest in mouse oocyte. However, roles of 14-3-3ε in the mitosis of fertilized mouse eggs have remained unclear. Here, we showed that 14-3-3ε interacts and cooperates with CDC25B phosphorylated at Ser321 regulating G2/M transition of mitotic progress of fertilized mouse eggs. Disruption of 14-3-3ε expression by RNAi prevented normal G2/M transition by inhibition of MPF activity and leaded to the translocation of CDC25B into the nucleus from the cytoplasm. Overexpression of 14-3-3ε-WT and unphosphorylatable CDC25B mutant (CDC25B-S321A) induced mitotic resumption in dbcAMP-arrested eggs. In addition, we examined endogenous and exogenous distribution of 14-3-3ε and CDC25B. Endogenous 14-3-3ε and CDC25B were co-localized primarily in the cytoplasm at the G1, S, early G2 and M phases whereas CDC25B was found to accumulate in the nucleus at the late G2 phase. Upon coexpression with RFP–14-3-3ε, GFP–CDC25B–WT and GFP–CDC25B–S321A were predominantly cytoplasmic at early G2 phase and then GFP–CDC25B–S321A moved to the nucleus whereas CDC25B-WT signals were observed in the cytoplasm without nucleus accumulation at late G2 phase at presence of dbcAMP. Our data indicate that 14-3-3ε is required for the mitotic entry in the fertilized mouse eggs. 14-3-3ε is primarily responsible for sequestering the CDC25B in cytoplasm and 14-3-3ε binding to CDC25B-S321 phosphorylated by PKA induces mitotic arrest at one-cell stage by inactivation of MPF in fertilized mouse eggs.
Tài liệu tham khảo
McGowan CH, Russell P: Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. EMBO J. 1993, 12: 75-85.
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.
Parker LL, Piwnica-Worms H: Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science. 1992, 257: 1955-1957.
Morgan DO: Principles of CDK regulation. Nature. 1995, 374: 131-134.
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: 242-245.
Donzelli M, Draetta GF: Regulating mammalian checkpoints through Cdc25 inactivation. EMBO Rep. 2003, 4: 671-677.
Trinkle-Mulcahy L, Lamond AI: Mitotic phosphatases: no longer silent partners. Curr Opin Cell Biol. 2006, 18: 623-631.
Nishijima H, Nishitani H, Seki T, Nishimoto T: A dual-specificity phosphatase Cdc25B is an unstable protein and triggers p34 (cdc2)/cyclin B activation in hamster BHK21 cells arrested with hydroxyurea. J Cell Biol. 1997, 138: 1105-1116.
Cui C, Zhao H, Zhang Z, Zong Z, Feng C, Zhang Y, Deng X, Xu X, Yu B: CDC25B acts as a potential target of PRKACA in fertilized mouse eggs. Biol Reprod. 2008, 79: 991-998.
Xiao J, Liu C, Hou J, Cui C, Wu D, Fan H, Sun X, Meng J, Yang F, Wang E, Yu B: Ser149 is another potential PKA phosphorylation target of Cdc25B in G2/M transition of fertilized mouse eggs. J Biol Chem. 2011, 286: 10356-10366.
Jin J, Smith FD, Stark C, Wells CD, Fawcett JP, Kulkarni S, Metalnikov P, O'Donnell P, Taylor P, Taylor L, Zougman A, Woodgett JR, Langeberg LK, Scott JD, Pawson T: Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr Biol. 2004, 14: 1436-1450.
Mackintosh C: Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J. 2004, 381: 329-342.
Dougherty MK, Morrison DK: Unlocking the code of 14-3-3. J Cell Sci. 2004, 117: 1875-1884.
Aitken A: 14-3-3 proteins: a historic overview. Semin Cancer Biol. 2006, 16: 162-172.
Chaudhri M, Scarabel M, Aitken A: Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem Biophys Res Commun. 2003, 300: 679-685.
Du J, Chen L, Luo X, Shen Y, Dou Z, Shen J, Cheng L, Chen Y, Li C, Wang H, Yao X: 14-3-3zeta cooperates with phosphorylated Plk1 and is required for correct cytokinesis. Front Biosci (Schol Ed). 2012, 4: 639-650.
Kosaka Y, Cieslik KA, Li L, Lezin G, Maguire CT, Saijoh Y, Toyo-oka K, Gambello MJ, Vatta M, Wynshaw-Boris A, Baldini A, Yost HJ, Brunelli L: 14-3-3ε plays a role in cardiac ventricular compaction by regulating the cardiomyocyte cell cycle. Mol Cell Biol. 2012, 32: 5089-5102.
De S, Marcinkiewicz JL, Vijayaraghavan S, Kline D: Expression of 14-3-3 protein isoforms in mouse oocytes, eggs and ovarian follicular development. BMC Res Notes. 2012, 5: 57-doi:10.1186/1756-0500-5-57
De S, Kline D: Evidence for the requirement of 14-3-3eta (YWHAH) in meiotic spindle assembly during mouse oocyte maturation. BMC Dev Biol. 2013, 13: 10-doi:10.1186/1471-213X-13-10
Forrest A, Gabrielli B: Cdc25B activity is regulated by 14-3-3. Oncogene. 2001, 20: 4393-4401.
Astuti P, Boutros R, Ducommun B, Gabrielli B: Mitotic phosphorylation of Cdc25B Ser321 disrupts 14-3-3 binding to the high affinity Ser323 site. J Biol Chem. 2010, 285: 34364-34370.
Pirino G, Wescott MP, Donovan PJ: Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle. 2009, 8: 665-670.
Meng J, Cui C, Liu Y, Jin M, Wu D, Liu C, Wang E, Yu B: The role of 14-3-3ε interaction with phosphorylated Cdc25B at its Ser321 in the release of the mouse oocyte from prophase I arrest. PLoS One. 2013, 8: e53633-
Tzivion G, Avruch J: 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation. J Biol Chem. 2002, 277: 3061-3064.
Gardino AK, Yaffe MB: 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol. 2011, 22: 688-695.
Wilker EW, van Vugt MA, Artim SA, Huang PH, Petersen CP, Reinhardt HC, Feng Y, Sharp PA, Sonenberg N, White FM, Yaffe MB: 14-3-3sigma controls mitotic translation to facilitate cytokinesis. Nature. 2007, 446: 329-332.
Saurin AT, Durgan J, Cameron AJ, Faisal A, Marber MS, Parker PJ: The regulated assembly of a PKC epsilon complex controls the completion of cytokinesis. Nat Cell Biol. 2008, 10: 891-901.
Chen D, Zhang Y, Yi Q, Huang Y, Hou H, Zhang Y, Hao Q, Cooke HJ, Li L, Sun Q, Shi Q: Regulation of asymmetrical cytokinesis by cAMP during meiosis I in mouse oocytes. PLoS One. 2012, 7: e29735-
Schultz RM, Montgomery RR, Belanoff JR: Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol. 1983, 97: 264-273.
Liu C, Liu Y, Liu Y, Wu D, Luan Z, Wang E, Yu B: Ser 15 of WEE1B is a potential PKA phosphorylation target in G2/M transition in one-cell stage mouse embryos. Mol Med Rep. 2013, 7: 1929-1937.
Davezac N, Baldin V, Gabrielli B, Forrest A, Theis-Febvre N, Yashida M, Ducommun B: Regulation of CDC25B phosphatases subcellular localization. Oncogene. 2000, 19: 2179-2185.
Lindqvist A, Källström H, Karlsson Rosenthal C: Characterisation of Cdc25B localisation and nuclear export during the cell cycle and in response to stress. J Cell Sci. 2004, 117: 4979-4990.
Karlsson C, Katich S, Hagting A, Hoffmann I, Pines J: Cdc25B and Cdc25C differ markedly in their properties as initiators of mitosis. J Cell Biol. 1999, 146 (3): 573-584.
Uchida S, Kuma A, Ohtsubo M, Shimura M, Hirata M, Nakagama H, Matsunaga T, Ishizaka Y, Yamashita K: Binding of 14-3-3beta but not 14-3-3sigma controls the cytoplasmic localization of CDC25B: binding site preferences of 14-3-3 subtypes and the subcellular localization of CDC25B. J Cell Sci. 2004, 117: 3011-3020.
Graves PR, Lovly CM, Uy GL, Piwnica-Worms H: Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding. Oncogene. 2001, 20: 1839-1851.
Kumagai A, Dunphy WG: Binding of 14-3-3 proteins and nuclear export control the intracellular localization of the mitotic inducer Cdc25. Genes Dev. 1999, 13: 1067-1072.
Ogg S, Gabrielli B, Piwnica-Worms H: Purification of a serine kinase that associates with and phosphorylates human Cdc25C on serine 216. J Biol Chem. 1994, 269: 30461-30469.
Margolis SS, Walsh S, Weiser DC, Yoshida M, Shenolikar S, Kornbluth S: PP1 control of M phase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation. EMBO J. 2003, 22: 5734-5745.
Margolis SS, Kornbluth S: When the checkpoints have gone: insights into Cdc25 functional activation. Cell Cycle. 2004, 3: 425-428.
De Souza CP, Ellem KA, Gabrielli BG: Centrosomal and cytoplasmic Cdc2/cyclin B1 activation precedes nuclear mitotic events. Exp Cell Res. 2000, 257: 11-21.
Jackman M, Lindon C, Nigg EA, Pines J: Active cyclin B1–Cdk1 first appears on centrosomes in prophase. Nat Cell Biol. 2003, 5: 143-148.
Krämer A, Mailand N, Lukas C, Syljuåsen RG, Wilkinson CJ, Nigg EA, Bartek J, Lukas J: Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol. 2004, 6: 884-891.
Meek SE, Lane WS, Piwnica-Worms H: Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J Biol Chem. 2004, 279: 32046-32054.
Pozuelo Rubio M, Geraghty KM, Wong BH, Wood NT, Campbell DG, Morrice N, Mackintosh C: 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem J. 2004, 379: 395-408.
Hogan B, Constantini LE: Manipulating the mouse embryo: a laboratory manual. 1986, Cold Harbor Laboratory Press, New York
Zhang Z, Su WH, Feng C, Yu DH, Cui C, Xu XY, Yu BZ: Polo-like kinase 1 may regulate G2/M transition of mouse fertilized eggs by means of inhibiting the phosphorylation of Tyr 15 of Cdc2. Mol Reprod Dev. 2007, 74: 1247-1254.
Gallicano GI, McGaughey RW, Capco DG: Activation of protein kinase C after fertilization is required for remodeling the mouse egg into the zygote. Mol Reprod Dev. 1997, 46: 587-601.