Skip to main content
SpringerLink
Log in

Protein Kinases and Protein Phosphatases that Regulate Meiotic Maturation in Mouse Oocytes

  • Chapter
  • First Online:
Cell Cycle in Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS))

Abstract

Oocytes arrest at prophase of meiosis I (MI) and in vivo do not resume meiosis until they receive ovulatory cues. Meiotic resumption entails two rounds of chromosome segregation without an intervening round of DNA replication and an arrest at metaphase of meiosis II (MII); fertilization triggers exit from MII and entry into interphase. During meiotic resumption, there is a burst of protein phosphorylation and dephosphorylation that dramatically changes during the course of oocyte meiotic maturation. Many of these phosphorylation and dephosphorylation events are key to regulating meiotic cell cycle arrest and/or progression, chromosome dynamics, and meiotic spindle assembly and disassembly. This review, which is subdivided into sections based upon meiotic cell cycle stages, focuses on the major protein kinases and phosphatases that have defined requirements during meiosis in mouse oocytes and, when possible, connects these regulatory pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alessi DR, Caudwell FB, Andjelkovic M, Hemmings BA, Cohen P (1996) Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett 399(3):333–338

    CAS  PubMed  Google Scholar 

  • Alexandru G, Uhlmann F, Mechtler K, Poupart MA, Nasmyth K (2001) Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105(4):459–472

    CAS  PubMed  Google Scholar 

  • Archambault V, Glover DM (2009) Polo-like kinases: conservation and divergence in their functions and regulation. Nat Rev Mol Cell Biol 10(4):265–275

    CAS  PubMed  Google Scholar 

  • Backs J, Backs T, Neef S, Kreusser MM, Lehmann LH, Patrick DM, Grueter CE, Qi X, Richardson JA, Hill JA, Katus HA, Bassel-Duby R, Maier LS, Olson EN (2009) The delta isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload. Proc Natl Acad Sci USA 106(7):2342–2347

    CAS  PubMed  Google Scholar 

  • Backs J, Stein P, Backs T, Duncan FE, Grueter CE, McAnally J, Qi X, Schultz RM, Olson EN (2010) The gamma isoform of CaM kinase II controls mouse egg activation by regulating cell cycle resumption. Proc Natl Acad Sci USA 107(1):81–86

    CAS  PubMed  Google Scholar 

  • Baluch DP, Capco DG (2008) GSK3 beta mediates acentromeric spindle stabilization by activated PKC zeta. Dev Biol 317(1):46–58

    CAS  PubMed  Google Scholar 

  • Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M (2008) The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 134(2):256–267

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beaumont HM, Mandl AM (1961) A quantitative and cytological study of oogonia and oocytes in the foetal and neonatal rat. Proc R Soc London B 155:557–579

    Google Scholar 

  • Berdougo E, Nachury MV, Jackson PK, Jallepalli PV (2008) The nucleolar phosphatase Cdc14B is dispensable for chromosome segregation and mitotic exit in human cells. Cell Cycle 7(9):1184–1190

    CAS  PubMed  Google Scholar 

  • Bischoff JR, Anderson L, Zhu Y, Mossie K, Ng L, Souza B, Schryver B, Flanagan P, Clairvoyant F, Ginther C, Chan CS, Novotny M, Slamon DJ, Plowman GD (1998) A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. Embo J 17(11):3052–3065

    CAS  PubMed  Google Scholar 

  • Bornslaeger EA, Mattei P, Schultz RM (1986) Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation. Dev Biol 114(2):453–462

    CAS  PubMed  Google Scholar 

  • Bornslaeger EA, Mattei PM, Schultz RM (1988) Protein phosphorylation in meiotically competent and incompetent mouse oocytes. Mol Reprod Dev 1(1):19–25

    CAS  PubMed  Google Scholar 

  • Brar GA, Amon A (2008) Emerging roles for centromeres in meiosis I chromosome segregation. Nat Rev Genet 9(12):899–910

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brar GA, Kiburz BM, Zhang Y, Kim JE, White F, Amon A (2006) Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441(7092):532–536

    CAS  PubMed  Google Scholar 

  • Brennan IM, Peters U, Kapoor TM, Straight AF (2007) Polo-like kinase controls vertebrate spindle elongation and cytokinesis. PLoS One 2(5):e409

    PubMed Central  PubMed  Google Scholar 

  • Brown JR, Koretke KK, Birkeland ML, Sanseau P, Patrick DR (2004) Evolutionary relationships of Aurora kinases: implications for model organism studies and the development of anti-cancer drugs. BMC Evol Biol 4(1):39

    PubMed Central  PubMed  Google Scholar 

  • Brunet S, Dumont J, Lee KW, Kinoshita K, Hikal P, Gruss OJ, Maro B, Verlhac MH (2008) Meiotic regulation of TPX2 protein levels governs cell cycle progression in mouse oocytes. PLoS One 3(10):e3338

    PubMed Central  PubMed  Google Scholar 

  • Buonomo SB, Rabitsch KP, Fuchs J, Gruber S, Sullivan M, Uhlmann F, Petronczki M, Toth A, Nasmyth K (2003) Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12, and SLK19. Dev Cell 4(5):727–739

    CAS  PubMed  Google Scholar 

  • Byskov AG (1974) Cell kinetic studies of follicular atresia in the mouse ovary. J Reprod Fertil 37(2):277–285

    CAS  PubMed  Google Scholar 

  • Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G (2004) The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 101(32):11707–11712

    CAS  PubMed  Google Scholar 

  • Carmena M, Riparbelli MG, Minestrini G, Tavares AM, Adams R, Callaini G, Glover DM (1998) Drosophila polo kinase is required for cytokinesis. J Cell Biol 143(3):659–671

    CAS  PubMed  Google Scholar 

  • Chang HY, Minahan K, Merriman JA, Jones KT (2009) Calmodulin-dependent protein kinase gamma 3 (CamKIIgamma3) mediates the cell cycle resumption of metaphase II eggs in mouse. Development 136(24):4077–4081

    CAS  PubMed  Google Scholar 

  • Chen MS, Hurov J, White LS, Woodford-Thomas T, Piwnica-Worms H (2001) Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol Cell Biol 21(12):3853–3861

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng KY, Lowe ED, Sinclair J, Nigg EA, Johnson LN (2003) The crystal structure of the human polo-like kinase-1 polo box domain and its phospho-peptide complex. Embo J 22(21):5757–5768

    CAS  PubMed  Google Scholar 

  • Cho HP, Liu Y, Gomez M, Dunlap J, Tyers M, Wang Y (2005) The dual-specificity phosphatase CDC14B bundles and stabilizes microtubules. Mol Cell Biol 25(11):4541–4551

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choi T, Aoki F, Mori M, Yamashita M, Nagahama Y, Kohmoto K (1991) Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113(3):789–795

    CAS  PubMed  Google Scholar 

  • Clyne RK, Katis VL, Jessop L, Benjamin KR, Herskowitz I, Lichten M, Nasmyth K (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5(5):480–485

    CAS  PubMed  Google Scholar 

  • Colledge WH, Carlton MB, Udy GB, Evans MJ (1994) Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 370(6484):65–68

    CAS  PubMed  Google Scholar 

  • Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Horner K, Jin C, Tsafriri A (2002) Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol 187(1–2):153–159

    CAS  PubMed  Google Scholar 

  • Coucouvanis EC, Sherwood SW, Carswell-Crumpton C, Spack EG, Jones PP (1993) Evidence that the mechanism of prenatal germ cell death in the mouse is apoptosis. Exp Cell Res 209(2):238–247

    CAS  PubMed  Google Scholar 

  • Dekel N, Beers WH (1978) Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins. Proc Natl Acad Sci USA 75(9):4369–4373

    CAS  PubMed  Google Scholar 

  • Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 161(2):267–280

    CAS  PubMed  Google Scholar 

  • Doble BW, Woodgett JR (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116(Pt 7):1175–1186

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dohadwala M, da Cruz e Silva EF, Hall FL, Williams RT, Carbonaro-Hall DA, Nairn AC, Greengard P, Berndt N (1994) Phosphorylation and inactivation of protein phosphatase 1 by cyclin-dependent kinases. Proc Natl Acad Sci USA 91(14):6408–6412

    CAS  PubMed  Google Scholar 

  • Ducibella T, Fissore R (2008) The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 315(2):257–279

    CAS  PubMed  Google Scholar 

  • Dummler B, Tschopp O, Hynx D, Yang ZZ, Dirnhofer S, Hemmings BA (2006) Life with a single isoform of Akt: mice lacking Akt2 and Akt3 are viable but display impaired glucose homeostasis and growth deficiencies. Mol Cell Biol 26(21):8042–8051

    CAS  PubMed Central  PubMed  Google Scholar 

  • Duncan FE, Moss SB, Williams CJ (2006) Knockdown of the cAMP-dependent protein kinase (PKA) Type Ialpha regulatory subunit in mouse oocytes disrupts meiotic arrest and results in meiotic spindle defects. Dev Dyn 235(11):2961–2968

    CAS  PubMed  Google Scholar 

  • Elia AE, Cantley LC, Yaffe MB (2003a) Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299(5610):1228–1231

    CAS  PubMed  Google Scholar 

  • Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, Hoepker K, Mohammad D, Cantley LC, Smerdon SJ, Yaffe MB (2003b) The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115(1):83–95

    CAS  PubMed  Google Scholar 

  • Eppig JJ (2001) Oocyte control of ovarian follicular development and function in mammals. Reproduction 122(6):829–838

    CAS  PubMed  Google Scholar 

  • Eppig JJ, Downs SM (1984) Chemical signals that regulate mammalian oocyte maturation. Biol Reprod 30(1):1–11

    CAS  PubMed  Google Scholar 

  • Eppig JJ, Telfer EE (1993) Isolation and culture of oocytes. Methods Enzymol 225:77–84

    CAS  PubMed  Google Scholar 

  • Eppig JJ, Freter RR, Ward-Bailey PF, Schultz RM (1983) Inhibition of oocyte maturation in the mouse: participation of cAMP, steroid hormones, and a putative maturation-inhibitory factor. Dev Biol 100(1):39–49

    CAS  PubMed  Google Scholar 

  • Eppig JJ, Peters AH, Telfer EE, Wigglesworth K (1993) Production of cumulus expansion enabling factor by mouse oocytes grown in vitro: preliminary characterization of the factor. Mol Reprod Dev 34(4):450–456

    CAS  PubMed  Google Scholar 

  • Frame S, Cohen P, Biondi RM (2001) A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7(6):1321–1327

    CAS  PubMed  Google Scholar 

  • Gautier J, Matsukawa T, Nurse P, Maller J (1989) Dephosphorylation and activation of Xenopus p34cdc2 protein kinase during the cell cycle. Nature 339(6226):626–629

    CAS  PubMed  Google Scholar 

  • Gavin AC, Tsukitani Y, Schorderet-Slatkine S (1991) Induction of M-phase entry of prophase-blocked mouse oocytes through microinjection of okadaic acid, a specific phosphatase inhibitor. Exp Cell Res 192(1):75–81

    CAS  PubMed  Google Scholar 

  • Gavin AC, Cavadore JC, Schorderet-Slatkine S (1994) Histone H1 kinase activity, germinal vesicle breakdown and M phase entry in mouse oocytes. J Cell Sci 107(Pt 1):275–283

    CAS  PubMed  Google Scholar 

  • 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(4):1247–1255

    CAS  PubMed  Google Scholar 

  • Gopalan G, Chan CS, Donovan PJ (1997) A novel mammalian, mitotic spindle-associated kinase is related to yeast and fly chromosome segregation regulators. J Cell Biol 138(3):643–656

    CAS  PubMed  Google Scholar 

  • Gopalan G, Gilbert DJ, Copeland NG, Jenkins NA, Donovan PJ (1998) Chromosome localization of two new mammalian kinases related to yeast and fly chromosome segregation-regulators. Mamm Genome 9(1):86–87

    CAS  PubMed  Google Scholar 

  • Gorr IH, Reis A, Boos D, Wuhr M, Madgwick S, Jones KT, Stemmann O (2006) Essential CDK1-inhibitory role for separase during meiosis I in vertebrate oocytes. Nat Cell Biol 8(9):1035–1037

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gray CH, Good VM, Tonks NK, Barford D (2003) The structure of the cell cycle protein Cdc14 reveals a proline-directed protein phosphatase. Embo J 22(14):3524–3535

    CAS  PubMed  Google Scholar 

  • Hampl A, Eppig JJ (1995) Translational regulation of the gradual increase in histone H1 kinase activity in maturing mouse oocytes. Mol Reprod Dev 40(1):9–15

    CAS  PubMed  Google Scholar 

  • Han SJ, Chen R, Paronetto MP, Conti M (2005) Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 15(18):1670–1676

    CAS  PubMed  Google Scholar 

  • Han SJ, Vaccari S, Nedachi T, Andersen CB, Kovacina KS, Roth RA, Conti M (2006) Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. Embo J 25(24):5716–5725

    CAS  PubMed  Google Scholar 

  • Hanna CB, Yao S, Patta MC, Jensen JT, Wu X (2010) WEE2 is an oocyte-specific meiosis inhibitor in Rhesus Macaque monkeys. Biol Reprod 82(6):1190–1197

    CAS  PubMed  Google Scholar 

  • Hartwell LH, Culotti J, Pringle JR, Reid BJ (1974) Genetic control of the cell division cycle in yeast. Science 183(120):46–51

    CAS  PubMed  Google Scholar 

  • Harwood AJ (2001) Regulation of GSK-3: a cellular multiprocessor. Cell 105(7):821–824

    CAS  PubMed  Google Scholar 

  • Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takeda N, Ikawa Y et al (1994) Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370(6484):68–71

    CAS  PubMed  Google Scholar 

  • Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, van Meel J, Rieder CL, Peters JM (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161(2):281–294

    CAS  PubMed  Google Scholar 

  • 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(3):e69

    PubMed Central  PubMed  Google Scholar 

  • Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR (2000) Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406(6791):86–90

    CAS  PubMed  Google Scholar 

  • Hoffmann S, Tsurumi C, Kubiak JZ, Polanski Z (2006) Germinal vesicle material drives meiotic cell cycle of mouse oocyte through the 3’UTR-dependent control of cyclin B1 synthesis. Dev Biol 292(1):46–54

    CAS  PubMed  Google Scholar 

  • Holland AJ, Taylor SS (2006) Cyclin-B1-mediated inhibition of excess separase is required for timely chromosome disjunction. J Cell Sci 119(Pt 16):3325–3336

    CAS  PubMed  Google Scholar 

  • Hornig NC, Uhlmann F (2004) Preferential cleavage of chromatin-bound cohesin after targeted phosphorylation by Polo-like kinase. Embo J 23(15):3144–3153

    CAS  PubMed  Google Scholar 

  • Jaspersen SL, Charles JF, Tinker-Kulberg RL, Morgan DO (1998) A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol Biol Cell 9(10):2803–2817

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jinno S, Suto K, Nagata A, Igarashi M, Kanaoka Y, Nojima H, Okayama H (1994) Cdc25A is a novel phosphatase functioning early in the cell cycle. Embo J 13(7):1549–1556

    CAS  PubMed  Google Scholar 

  • Kaiser BK, Zimmerman ZA, Charbonneau H, Jackson PK (2002) Disruption of centrosome structure, chromosome segregation, and cytokinesis by misexpression of human Cdc14A phosphatase. Mol Biol Cell 13(7):2289–2300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kakizuka A, Sebastian B, Borgmeyer U, Hermans-Borgmeyer I, Bolado J, Hunter T, Hoekstra MF, Evans RM (1992) A mouse cdc25 homolog is differentially and developmentally expressed. Genes Dev 6(4):578–590

    CAS  PubMed  Google Scholar 

  • Kalous J, Solc P, Baran V, Kubelka M, Schultz RM, Motlik J (2006) PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol Cell 98(2):111–123

    CAS  PubMed  Google Scholar 

  • Kar S, Adachi T, Carr BI (2002) EGFR-independent activation of ERK1/2 mediates growth inhibition by a PTPase antagonizing K-vitamin analog. J Cell Physiol 190(3):356–364

    CAS  PubMed  Google Scholar 

  • Karaiskou A, Cayla X, Haccard O, Jessus C, Ozon R (1998) MPF amplification in Xenopus oocyte extracts depends on a two-step activation of cdc25 phosphatase. Exp Cell Res 244(2):491–500

    CAS  PubMed  Google Scholar 

  • Kemp BE, Parker MW, Hu S, Tiganis T, House C (1994) Substrate and pseudosubstrate interactions with protein kinases: determinants of specificity. Trends Biochem Sci 19(11):440–444

    CAS  PubMed  Google Scholar 

  • Kim S, Jee K, Kim D, Koh H, Chung J (2001) Cyclic AMP inhibits Akt activity by blocking the membrane localization of PDK1. J Biol Chem 276(16):12864–12870

    CAS  PubMed  Google Scholar 

  • Kim LC, Song L, Haura EB (2009) Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 6(10):587–595

    PubMed  Google Scholar 

  • Kimmins S, Crosio C, Kotaja N, Hirayama J, Monaco L, Hoog C, van Duin M, Gossen JA, Sassone-Corsi P (2007) Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol Endocrinol 21(3):726–739

    CAS  PubMed  Google Scholar 

  • Kimura M, Matsuda Y, Yoshioka T, Okano Y (1999) Cell cycle-dependent expression and centrosome localization of a third human aurora/Ipl1-related protein kinase, AIK3. J Biol Chem 274(11):7334–7340

    CAS  PubMed  Google Scholar 

  • King WG, Mattaliano MD, Chan TO, Tsichlis PN, Brugge JS (1997) Phosphatidylinositol 3-kinase is required for integrin-stimulated AKT and Raf-1/mitogen-activated protein kinase pathway activation. Mol Cell Biol 17(8):4406–4418

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirschner LS, Yin Z, Jones GN, Mahoney E (2009) Mouse models of altered protein kinase A signaling. Endocr Relat Cancer 16(3):773–793

    CAS  PubMed  Google Scholar 

  • 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(7089):46–52

    CAS  PubMed  Google Scholar 

  • Knott JG, Gardner AJ, Madgwick S, Jones KT, Williams CJ, Schultz RM (2006) Calmodulin-dependent protein kinase II triggers mouse egg activation and embryo development in the absence of Ca2+ oscillations. Dev Biol 296(2):388–395

    CAS  PubMed  Google Scholar 

  • Kramer ER, Scheuringer N, Podtelejnikov AV, Mann M, Peters JM (2000) Mitotic regulation of the APC activator proteins CDC20 and CDH1. Mol Biol Cell 11(5):1555–1569

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kubiak JZ, Weber M, de Pennart H, Winston NJ, Maro B (1993) The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. Embo J 12(10):3773–3778

    CAS  PubMed  Google Scholar 

  • Kume S, Endo T, Nishimura Y, Kano K, Naito K (2007) Porcine SPDYA2 (RINGO A2) stimulates CDC2 activity and accelerates meiotic maturation of porcine oocytes. Biol Reprod 76(3):440–447

    CAS  PubMed  Google Scholar 

  • Labbe JC, Capony JP, Caput D, Cavadore JC, Derancourt J, Kaghad M, Lelias JM, Picard A, Doree M (1989a) MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. Embo J 8(10):3053–3058

    CAS  PubMed  Google Scholar 

  • Labbe JC, Picard A, Peaucellier G, Cavadore JC, Nurse P, Doree M (1989b) Purification of MPF from starfish: identification as the H1 histone kinase p34cdc2 and a possible mechanism for its periodic activation. Cell 57(2):253–263

    CAS  PubMed  Google Scholar 

  • Lammer C, Wagerer S, Saffrich R, Mertens D, Ansorge W, Hoffmann I (1998) The cdc25B phosphatase is essential for the G2/M phase transition in human cells. J Cell Sci 111(Pt 16):2445–2453

    CAS  PubMed  Google Scholar 

  • Lee BH, Amon A (2003) Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300(5618):482–486

    CAS  PubMed  Google Scholar 

  • Levi M, Maro B, Shalgi R (2010) The involvement of Fyn kinase in resumption of the first meiotic division in mouse oocytes. Cell Cycle 9(8):1577–1589

    Google Scholar 

  • Lincoln AJ, Wickramasinghe D, Stein P, Schultz RM, Palko ME, De Miguel MP, Tessarollo L, Donovan PJ (2002) Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 30(4):446–449

    CAS  PubMed  Google Scholar 

  • Lindqvist A, Kallstrom H, Lundgren A, Barsoum E, Rosenthal CK (2005) Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. J Cell Biol 171(1):35–45

    CAS  PubMed  Google Scholar 

  • Lindqvist A, Rodriguez-Bravo V, Medema RH (2009) The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J Cell Biol 185(2):193–202

    CAS  PubMed  Google Scholar 

  • Llano E, Gomez R, Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Vazquez-Quinones L, Hernandez T, de Alava E, Cuadrado A, Barbero JL, Suja JA, Pendas AM (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22(17):2400–2413

    CAS  PubMed  Google Scholar 

  • Lohka MJ (1998) Nuclear responses to MPF activation and inactivation in Xenopus oocytes and early embryos. Biol Cell 90(8):591–599

    CAS  PubMed  Google Scholar 

  • Macurek L, Lindqvist A, Lim D, Lampson MA, Klompmaker R, Freire R, Clouin C, Taylor SS, Yaffe MB, Medema RH (2008) Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455(7209):119–123

    CAS  PubMed  Google Scholar 

  • Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT (2006) Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J Cell Biol 174(6):791–801

    CAS  PubMed  Google Scholar 

  • Mailand N, Lukas C, Kaiser BK, Jackson PK, Bartek J, Lukas J (2002) Deregulated human Cdc14A phosphatase disrupts centrosome separation and chromosome segregation. Nat Cell Biol 4(4):317–322

    CAS  PubMed  Google Scholar 

  • Mailhes JB, Hilliard C, Fuseler JW, London SN (2003) Okadaic acid, an inhibitor of protein phosphatase 1 and 2A, induces premature separation of sister chromatids during meiosis I and aneuploidy in mouse oocytes in vitro. Chromosome Res 11(6):619–631

    CAS  PubMed  Google Scholar 

  • Manning BD, Cantley LC (2007) AKT/PKB signaling: navigating downstream. Cell 129(7):1261–1274

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marangos P, Carroll J (2004) The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction 128(2):153–162

    CAS  PubMed  Google Scholar 

  • Marston AL, Lee BH, Amon A (2003) The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation. Dev Cell 4(5):711–726

    CAS  PubMed  Google Scholar 

  • Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V (2004) Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 114(2):196–205

    CAS  PubMed Central  PubMed  Google Scholar 

  • Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57:185–282

    CAS  PubMed  Google Scholar 

  • McCollum D (2004) Cytokinesis: the central spindle takes center stage. Curr Biol 14(22):R953–R955

    CAS  PubMed  Google Scholar 

  • McGinnis LK, Albertini DF, Kinsey WH (2007) Localized activation of Src-family protein kinases in the mouse egg. Dev Biol 306(1):241–254

    CAS  PubMed Central  PubMed  Google Scholar 

  • McGinnis LK, Kinsey WH, Albertini DF (2009) Functions of Fyn kinase in the completion of meiosis in mouse oocytes. Dev Biol 327(2):280–287

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, Pendola FL, Knowles BB, Eppig JJ, Jaffe LA (2004) The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306(5703):1947–1950

    CAS  PubMed  Google Scholar 

  • Minshull J, Straight A, Rudner AD, Dernburg AF, Belmont A, Murray AW (1996) Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr Biol 6(12):1609–1620

    CAS  PubMed  Google Scholar 

  • Mitchell AP, Bowdish KS (1992) Selection for early meiotic mutants in yeast. Genetics 131(1):65–72

    CAS  PubMed  Google Scholar 

  • Mitchell AP, Driscoll SE, Smith HE (1990) Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol Cell Biol 10(5):2104–2110

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mitra J, Schultz RM (1996) Regulation of the acquisition of meiotic competence in the mouse: changes in the subcellular localization of cdc2, cyclin B1, cdc25C and wee1, and in the concentration of these proteins and their transcripts. J Cell Sci 109(Pt 9):2407–2415

    CAS  PubMed  Google Scholar 

  • 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(4):631–639

    CAS  PubMed  Google Scholar 

  • Moore GP (1975) The RNA polymerase activity of the preimplantation mouse embryo. J Embryol Exp Morphol 34(2):291–298

    CAS  PubMed  Google Scholar 

  • Moore GP, Lintern-Moore S (1978) Transcription of the mouse oocyte genome. Biol Reprod 18(5):865–870

    CAS  PubMed  Google Scholar 

  • Morgan DO (1995) Principles of CDK regulation. Nature 374(6518):131–134

    CAS  PubMed  Google Scholar 

  • Murray AW, Solomon MJ, Kirschner MW (1989) The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339(6222):280–286

    CAS  PubMed  Google Scholar 

  • Nagata A, Igarashi M, Jinno S, Suto K, Okayama H (1991) An additional homolog of the fission yeast cdc25+ gene occurs in humans and is highly expressed in some cancer cells. New Biol 3(10):959–968

    CAS  PubMed  Google Scholar 

  • Nemoto K, Vogt A, Oguri T, Lazo JS (2004) Activation of the Raf-1/MEK/Erk kinase pathway by a novel Cdc25 inhibitor in human prostate cancer cells. Prostate 58(1):95–102

    CAS  PubMed  Google Scholar 

  • Nguyen HG, Chinnappan D, Urano T, Ravid K (2005) Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol Cell Biol 25(12):4977–4992

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nurse P (1990) Universal control mechanism regulating onset of M-phase. Nature 344(6266):503–508

    CAS  PubMed  Google Scholar 

  • Oh JS, Han SJ, Conti M (2010) Wee1B, Myt1, and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic resumption. J Cell Biol 188(2):199–207

    CAS  PubMed  Google Scholar 

  • Pahlavan G, Polanski Z, Kalab P, Golsteyn R, Nigg EA, Maro B (2000) Characterization of polo-like kinase 1 during meiotic maturation of the mouse oocyte. Dev Biol 220(2):392–400

    CAS  PubMed  Google Scholar 

  • Parry DH, O’Farrell PH (2001) The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Curr Biol 11(9):671–683

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pesty A, Lefevre B, Kubiak J, Geraud G, Tesarik J, Maro B (1994) Mouse oocyte maturation is affected by lithium via the polyphosphoinositide metabolism and the microtubule network. Mol Reprod Dev 38(2):187–199

    CAS  PubMed  Google Scholar 

  • Peter M, Nakagawa J, Doree M, Labbe JC, Nigg EA (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61(4):591–602

    CAS  PubMed  Google Scholar 

  • Pirino G, Wescott MP, Donovan PJ (2009) Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 8(4):665–670

    CAS  PubMed  Google Scholar 

  • Rayasam GV, Tulasi VK, Sodhi R, Davis JA, Ray A (2009) Glycogen synthase kinase 3: more than a namesake. Br J Pharmacol 156(6):885–898

    CAS  PubMed  Google Scholar 

  • Reis A, Chang HY, Levasseur M, Jones KT (2006) APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nat Cell Biol 8(5):539–540

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reis A, Madgwick S, Chang HY, Nabti I, Levasseur M, Jones KT (2007) Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nat Cell Biol 9(10):1192–1198

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rime H, Ozon R (1990) Protein phosphatases are involved in the in vivo activation of histone H1 kinase in mouse oocyte. Dev Biol 141(1):115–122

    CAS  PubMed  Google Scholar 

  • Roy J, Cyert MS (2009) Cracking the phosphatase code: docking interactions determine substrate specificity. Sci Signal 2(100):re9

    PubMed  Google Scholar 

  • Ruiz EJ, Hunt T, Nebreda AR (2008) Meiotic inactivation of Xenopus Myt1 by CDK/XRINGO, but not CDK/cyclin, via site-specific phosphorylation. Mol Cell 32(2):210–220

    CAS  PubMed  Google Scholar 

  • Russell P, Nurse P (1986) cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45(1):145–153

    CAS  PubMed  Google Scholar 

  • Sadhu K, Reed SI, Richardson H, Russell P (1990) Human homolog of fission yeast cdc25 mitotic inducer is predominantly expressed in G2. Proc Natl Acad Sci USA 87(13):5139–5143

    CAS  PubMed  Google Scholar 

  • Sasai K, Katayama H, Stenoien DL, Fujii S, Honda R, Kimura M, Okano Y, Tatsuka M, Suzuki F, Nigg EA, Earnshaw WC, Brinkley WR, Sen S (2004) Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil Cytoskeleton 59(4):249–263

    CAS  PubMed  Google Scholar 

  • Saskova A, Solc P, Baran V, Kubelka M, Schultz RM, Motlik J (2008) Aurora kinase A controls meiosis I progression in mouse oocytes. Cell Cycle 7(15):2368–2376

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schaber M, Lindgren A, Schindler K, Bungard D, Kaldis P, Winter E (2002) CAK1 promotes meiosis and spore formation in Saccharomyces cerevisiae in a CDC28-independent fashion. Mol Cell Biol 22(1):57–68

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schindler K, Schultz RM (2009a) CDC14B acts through FZR1 (CDH1) to prevent meiotic maturation of mouse oocytes. Biol Reprod 80(4):795–803

    CAS  PubMed  Google Scholar 

  • Schindler K, Schultz RM (2009b) The CDC14A phosphatase regulates oocyte maturation in mouse. Cell Cycle 8(7):1090–1098

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schindler K, Benjamin KR, Martin A, Boglioli A, Herskowitz I, Winter E (2003) The Cdk-activating kinase Cak1p promotes meiotic S phase through Ime2p. Mol Cell Biol 23(23):8718–8728

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schmidt A, Rauh NR, Nigg EA, Mayer TU (2006) Cytostatic factor: an activity that puts the cell cycle on hold. J Cell Sci 119(Pt 7):1213–1218

    CAS  PubMed  Google Scholar 

  • Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130(3):484–498

    CAS  PubMed  Google Scholar 

  • Schultz RM, Montgomery RR, Belanoff JR (1983) Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 97(2):264–273

    CAS  PubMed  Google Scholar 

  • Schwartz DA, Schultz RM (1991) Stimulatory effect of okadaic acid, an inhibitor of protein phosphatases, on nuclear envelope breakdown and protein phosphorylation in mouse oocytes and one-cell embryos. Dev Biol 145(1):119–127

    CAS  PubMed  Google Scholar 

  • Sebastian B, Kakizuka A, Hunter T (1993) Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15. Proc Natl Acad Sci USA 90(8):3521–3524

    CAS  PubMed  Google Scholar 

  • Seki A, Coppinger JA, Jang CY, Yates JR, Fang G (2008) Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science 320(5883):1655–1658

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sen S, Zhou H, White RA (1997) A putative serine/threonine kinase encoding gene BTAK on chromosome 20q13 is amplified and overexpressed in human breast cancer cell lines. Oncogene 14(18):2195–2200

    CAS  PubMed  Google Scholar 

  • Sette C, Paronetto MP, Barchi M, Bevilacqua A, Geremia R, Rossi P (2002) Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. Embo J 21(20):5386–5395

    CAS  PubMed  Google Scholar 

  • Shou W, Seol JH, Shevchenko A, Baskerville C, Moazed D, Chen ZW, Jang J, Shevchenko A, Charbonneau H, Deshaies RJ (1999) Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 97(2):233–244

    CAS  PubMed  Google Scholar 

  • Shuda K, Schindler K, Ma J, Schultz RM, Donovan PJ (2009) Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol Reprod Dev 76(11):1094–1105

    CAS  PubMed Central  PubMed  Google Scholar 

  • Silva AJ, Paylor R, Wehner JM, Tonegawa S (1992a) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257(5067):206–211

    CAS  PubMed  Google Scholar 

  • Silva AJ, Stevens CF, Tonegawa S, Wang Y (1992b) Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257(5067):201–206

    CAS  PubMed  Google Scholar 

  • Simanis V (2003) Events at the end of mitosis in the budding and fission yeasts. J Cell Sci 116(Pt 21):4263–4275

    CAS  PubMed  Google Scholar 

  • Smith GD, Sadhu A, Mathies S, Wolf DP (1998) Characterization of protein phosphatases in mouse oocytes. Dev Biol 204(2):537–549

    CAS  PubMed  Google Scholar 

  • Solc P, Saskova A, Baran V, Kubelka M, Schultz RM, Motlik J (2008) CDC25A phosphatase controls meiosis I progression in mouse oocytes. Dev Biol 317(1):260–269

    CAS  PubMed Central  PubMed  Google Scholar 

  • Solc P, Schultz RM, Motlik J (2010) Prophase I arrest and progression to metaphase I in mouse oocytes: Comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Mol Hum Reprod 16(9):654–664

    CAS  PubMed  Google Scholar 

  • Sorensen RA, Wassarman PM (1976) Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol 50(2):531–536

    CAS  PubMed  Google Scholar 

  • 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(2):207–220

    CAS  PubMed  Google Scholar 

  • Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW (2001) Dual inhibition of sister chromatid separation at metaphase. Cell 107(6):715–726

    CAS  PubMed  Google Scholar 

  • Stemmann O, Gorr IH, Boos D (2006) Anaphase topsy-turvy: Cdk1 a securin, separase a CKI. Cell Cycle 5(1):11–13

    CAS  PubMed  Google Scholar 

  • Stricker SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211(2):157–176

    CAS  PubMed  Google Scholar 

  • Su YQ, Denegre JM, Wigglesworth K, Pendola FL, O’Brien MJ, Eppig JJ (2003) Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus cell complex. Dev Biol 263(1):126–138

    CAS  PubMed  Google Scholar 

  • Sumara I, Gimenez-Abian JF, Gerlich D, Hirota T, Kraft C, de la Torre C, Ellenberg J, Peters JM (2004) Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr Biol 14(19):1712–1722

    CAS  PubMed  Google Scholar 

  • Swain JE, Wang X, Saunders TL, Dunn R, Smith GD (2003) Specific inhibition of mouse oocyte nuclear protein phosphatase-1 stimulates germinal vesicle breakdown. Mol Reprod Dev 65(1):96–103

    CAS  PubMed  Google Scholar 

  • Swain JE, Ding J, Wu J, Smith GD (2008) Regulation of spindle and chromatin dynamics during early and late stages of oocyte maturation by aurora kinases. Mol Hum Reprod 14(5):291–299

    CAS  PubMed  Google Scholar 

  • Talmor-Cohen A, Tomashov-Matar R, Tsai WB, Kinsey WH, Shalgi R (2004) Fyn kinase-tubulin interaction during meiosis of rat eggs. Reproduction 128(4):387–393

    CAS  PubMed  Google Scholar 

  • Tay J, Hodgman R, Richter JD (2000) The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol 221(1):1–9

    CAS  PubMed  Google Scholar 

  • Terret ME, Ferby I, Nebreda AR, Verlhac MH (2001) RINGO efficiently triggers meiosis resumption in mouse oocytes and induces cell cycle arrest in embryos. Biol Cell 93(1–2):89–97

    CAS  PubMed  Google Scholar 

  • Tong C, Fan HY, Lian L, Li SW, Chen DY, Schatten H, Sun QY (2002) Polo-like kinase-1 is a pivotal regulator of microtubule assembly during mouse oocyte meiotic maturation, fertilization, and early embryonic mitosis. Biol Reprod 67(2):546–554

    CAS  PubMed  Google Scholar 

  • Tsafriri A, Chun SY, Zhang R, Hsueh AJ, Conti M (1996) Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev Biol 178(2):393–402

    CAS  PubMed  Google Scholar 

  • Tseng TC, Chen SH, Hsu YP, Tang TK (1998) Protein kinase profile of sperm and eggs: cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol 17(10):823–833

    CAS  PubMed  Google Scholar 

  • van Woerden GM, Hoebeek FE, Gao Z, Nagaraja RY, Hoogenraad CC, Kushner SA, Hansel C, De Zeeuw CI, Elgersma Y (2009) BetaCaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses. Nat Neurosci 12(7):823–825

    PubMed  Google Scholar 

  • Verlhac MH, Kubiak JZ, Clarke HJ, Maro B (1994) Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120(4):1017–1025

    CAS  PubMed  Google Scholar 

  • Verlhac MH, Kubiak JZ, Weber M, Geraud G, Colledge WH, Evans MJ, Maro B (1996) Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122(3):815–822

    CAS  PubMed  Google Scholar 

  • Virshup DM, Shenolikar S (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol Cell 33(5):537–545

    CAS  PubMed  Google Scholar 

  • Visintin R, Prinz S, Amon A (1997) CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278(5337):460–463

    CAS  PubMed  Google Scholar 

  • Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, Amon A (1998) The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2(6):709–718

    CAS  PubMed  Google Scholar 

  • Visintin R, Hwang ES, Amon A (1999) Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 398(6730):818–823

    CAS  PubMed  Google Scholar 

  • Vivarelli E, Conti M, De Felici M, Siracusa G (1983) Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differ 12(5):271–276

    CAS  PubMed  Google Scholar 

  • Vogt E, Kipp A, Eichenlaub-Ritter U (2009) Aurora kinase B, epigenetic state of centromeric heterochromatin and chiasma resolution in oocytes. Reprod Biomed Online 19(3):352–368

    CAS  PubMed  Google Scholar 

  • Wang X, Liu XT, Dunn R, Ohl DA, Smith GD (2003) Glycogen synthase kinase-3 regulates mouse oocyte homologue segregation. Mol Reprod Dev 64(1):96–105

    PubMed  Google Scholar 

  • Wang X, Swain JE, Bollen M, Liu XT, Ohl DA, Smith GD (2004) Endogenous regulators of protein phosphatase-1 during mouse oocyte development and meiosis. Reproduction 128(5):493–502

    CAS  PubMed  Google Scholar 

  • Wang Z, Zhang B, Wang M, Carr BI (2005) Cdc25A and ERK interaction: EGFR-independent ERK activation by a protein phosphatase Cdc25A inhibitor, compound 5. J Cell Physiol 204(2):437–444

    CAS  PubMed  Google Scholar 

  • Wang Y, Toppari J, Parvinen M, Kallio MJ (2006) Inhibition of Aurora kinases perturbs chromosome alignment and spindle checkpoint signaling in rat spermatocytes. Exp Cell Res 312(18):3459–3470

    CAS  PubMed  Google Scholar 

  • Welburn JP, Tucker JA, Johnson T, Lindert L, Morgan M, Willis A, Noble ME, Endicott JA (2007) How tyrosine 15 phosphorylation inhibits the activity of cyclin-dependent kinase 2-cyclin A. J Biol Chem 282(5):3173–3181

    CAS  PubMed  Google Scholar 

  • Wianny F, Tavares A, Evans MJ, Glover DM, Zernicka-Goetz M (1998) Mouse polo-like kinase 1 associates with the acentriolar spindle poles, meiotic chromosomes and spindle midzone during oocyte maturation. Chromosoma 107(6–7):430–439

    CAS  PubMed  Google Scholar 

  • Wu J, Cho HP, Rhee DB, Johnson DK, Dunlap J, Liu Y, Wang Y (2008) Cdc14B depletion leads to centriole amplification, and its overexpression prevents unscheduled centriole duplication. J Cell Biol 181(3):475–483

    CAS  PubMed  Google Scholar 

  • Xia K, Lee RS, Narsimhan RP, Mukhopadhyay NK, Neel BG, Roberts TM (1999) Tyrosine phosphorylation of the proto-oncoprotein Raf-1 is regulated by Raf-1 itself and the phosphatase Cdc25A. Mol Cell Biol 19(7):4819–4824

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu Z, Cetin B, Anger M, Cho US, Helmhart W, Nasmyth K, Xu W (2009) Structure and function of the PP2A-shugoshin interaction. Mol Cell 35(4):426–441

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamano H, Gannon J, Hunt T (1996) The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe. Embo J 15(19):5268–5279

    CAS  PubMed  Google Scholar 

  • Yanai A, Arama E, Kilfin G, Motro B (1997) ayk1, a novel mammalian gene related to Drosophila aurora centrosome separation kinase, is specifically expressed during meiosis. Oncogene 14(24):2943–2950

    CAS  PubMed  Google Scholar 

  • Yang KT, Li SK, Chang CC, Tang CJ, Lin YN, Lee SC, Tang TK (2010) Aurora-C kinase deficiency causes cytokinesis failure in meiosis i and production of large polyploid oocytes in mouse. Mol Biol Cell 21(14):2371–2383

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yuan K, Hu H, Guo Z, Fu G, Shaw AP, Hu R, Yao X (2007) Phospho-regulation of HsCdc14A By Polo-like kinase 1 is essential for mitotic progression. J Biol Chem 282(37):27414–27423

    CAS  PubMed  Google Scholar 

  • Zachariae W, Schwab M, Nasmyth K, Seufert W (1998) Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282(5394):1721–1724

    CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang Z, Xu XY, Li XS, Yu M, Yu AM, Zong ZH, Yu BZ (2008) Protein kinase A modulates Cdc25B activity during meiotic resumption of mouse oocytes. Dev Dyn 237(12):3777–3786

    CAS  PubMed  Google Scholar 

  • Zheng KG, Meng XQ, Yang Y, Yu YS, Liu DC, Li YL (2007) Requirements of Src family kinase during meiotic maturation in mouse oocyte. Mol Reprod Dev 74(1):125–130

    CAS  PubMed  Google Scholar 

  • 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(16):6196–6201

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Richard Schultz and Paula Stein for helpful discussions and critical reading of this review. This work is supported by a grant from the N.I.H. (HD061657 to KS and HD022681 to RS).

Author information

Authors and Affiliations

  1. Department of Biology, University of Pennsylvania, 433 S. University Avenue, Philadelphia, PA, 19104, USA

    Karen Schindler

Authors
  1. Karen Schindler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karen Schindler .

Editor information

Editors and Affiliations

  1. CNRS UMR 6061, Fac. Médecine, Université de Rennes 1, Rennes CX, 35043, France

    Jacek Z. Kubiak

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Schindler, K. (2011). Protein Kinases and Protein Phosphatases that Regulate Meiotic Maturation in Mouse Oocytes. In: Kubiak, J. (eds) Cell Cycle in Development. Results and Problems in Cell Differentiation. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19065-0_14

Download citation

Publish with us

Policies and ethics

Search

Navigation