The greatwall kinase is dominant over PKA in controlling the antagonistic function of ARPP19 in Xenopus oocytes

References

• Bontron S, Jaquenoud M, Vaga S, Talarek N, Bodenmiller B, Aebersold R, De Virgilio C. Yeast endosulfines control entry into quiescence and chronological life span by inhibiting protein phosphatase 2A. Cell Reports 2013; 3:16-22; PMID:23273919; https://doi.org/10.1016/j.celrep.2012.11.025
   PubMed Web of Science ®Google Scholar
• Talarek N, Bontron S, De Virgilio C. Quantification of mRNA stability of stress-responsive yeast genes following conditional excision of open reading frames. RNA Biol 2013; 10:1299-308; PMID:23792549; https://doi.org/10.4161/rna.25355
   PubMed Web of Science ®Google Scholar
• Talarek N, Cameroni E, Jaquenoud M, Luo X, Bontron S, Lippman S, Devgan G, Snyder M, Broach JR, De Virgilio C. Initiation of the TORC1-regulated G0 program requires Igo1/2, which license specific mRNAs to evade degradation via the 5′-3′ mRNA decay pathway. Mol Cell 2010; 38:345-55; PMID:20471941; https://doi.org/10.1016/j.molcel.2010.02.039
   PubMed Web of Science ®Google Scholar
• Juanes MA, Khoueiry R, Kupka T, Castro A, Mudrak I, Ogris E, Lorca T, Piatti S. Budding yeast greatwall and endosulfines control activity and spatial regulation of PP2A(Cdc55) for timely mitotic progression. PLoS Genet 2013; 9:e1003575; PMID:23861665; https://doi.org/10.1371/journal.pgen.1003575
   PubMed Web of Science ®Google Scholar
• White RE, Giffard RG. MicroRNA-320 induces neurite outgrowth by targeting ARPP-19. Neuroreport 2012; 23:590-5; PMID:22617447; https://doi.org/10.1097/WNR.0b013e3283540394
   PubMed Web of Science ®Google Scholar
• Jiang T, Zhao B, Li X, Wan J. ARPP-19 promotes proliferation and metastasis of human glioma. Neuroreport 2016; 27:960-6; PMID:27380244; https://doi.org/10.1097/WNR.0000000000000638
   PubMed Web of Science ®Google Scholar
• Vigneron S, Robert P, Hached K, Sundermann L, Charrasse S, Labbe JC, Castro A, Lorca T. The master Greatwall kinase, a critical regulator of mitosis and meiosis. Int J Dev Biol 2016; 60:245-54; PMID:27759153; https://doi.org/10.1387/ijdb.160155tl
   PubMed Web of Science ®Google Scholar
• Gharbi-Ayachi A, Labbe J-C, Burgess A, Vigneron S, Strub J-M, Brioudes E, Van-Dorsselaer A, Castro A, Lorca T. The Substrate of Greatwall Kinase, Arpp19, Controls Mitosis by Inhibiting Protein Phosphatase 2A. Science 2010; 330:1673-7; PMID:21164014; https://doi.org/10.1126/science.1197048
   PubMed Web of Science ®Google Scholar
• Mochida S, Maslen SL, Skehel M, Hunt T. Greatwall Phosphorylates an Inhibitor of Protein Phosphatase 2A That Is Essential for Mitosis. Science 2010; 330:1670-3; PMID:21164013; https://doi.org/10.1126/science.1195689
   PubMed Web of Science ®Google Scholar
• Yu J, Fleming SL, Williams B, Williams EV, Li Z, Somma P, Rieder CL, Goldberg ML. Greatwall kinase: a nuclear protein required for proper chromosome condensation and mitotic progression in Drosophila. J Cell Biol 2004; 164:487-92; PMID:14970188; https://doi.org/10.1083/jcb.200310059
   PubMed Web of Science ®Google Scholar
• Castilho PV, Williams BC, Mochida S, Zhao Y, Goldberg ML. The M phase kinase Greatwall (Gwl) promotes inactivation of PP2A/B55delta, a phosphatase directed against CDK phosphosites. Mol Biol Cell 2009; 20:4777-89; PMID:19793917; https://doi.org/10.1091/mbc.E09-07-0643
   PubMed Web of Science ®Google Scholar
• Mochida S, Ikeo S, Gannon J, Hunt T. Regulated activity of PP2A-B55delta is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J 2009; 28(18):2777-85; PMID:19696736; https://doi.org/10.1038/emboj.2009.238
   PubMed Web of Science ®Google Scholar
• Dupre A, Buffin E, Roustan C, Nairn AC, Jessus C, Haccard O. The phosphorylation of ARPP19 by Greatwall renders the auto-amplification of MPF independently of PKA in Xenopus oocytes. J Cell Sci 2013; 126:3916-26; PMID:23781026; https://doi.org/10.1242/jcs.126599
   PubMed Web of Science ®Google Scholar
• Rangone H, Wegel E, Gatt MK, Yeung E, Flowers A, Debski J, Dadlez M, Janssens V, Carpenter AT, Glover DM. Suppression of scant identifies Endos as a substrate of greatwall kinase and a negative regulator of protein phosphatase 2A in mitosis. PLoS Genet 2011; 7:e1002225; PMID:21852956; https://doi.org/10.1371/journal.pgen.1002225
   PubMed Web of Science ®Google Scholar
• Kim MY, Bucciarelli E, Morton DG, Williams BC, Blake-Hodek K, Pellacani C, Von Stetina JR, Hu X, Somma MP, Drummond-Barbosa D, et al. Bypassing the Greatwall-Endosulfine pathway: plasticity of a pivotal cell-cycle regulatory module in Drosophila melanogaster and Caenorhabditis elegans. Genetics 2012; 191:1181-97; PMID:22649080; https://doi.org/10.1534/genetics.112.140574
   PubMed Web of Science ®Google Scholar
• Labandera AM, Vahab AR, Chaudhuri S, Kerk D, Moorhead GB. The mitotic PP2A regulator ENSA/ARPP-19 is remarkably conserved across plants and most eukaryotes. Biochem Biophys Res Commun 2015; 458:739-44; PMID:25666948; https://doi.org/10.1016/j.bbrc.2015.01.123
   PubMed Web of Science ®Google Scholar
• Williams BC, Filter JJ, Blake-Hodek KA, Wadzinski BE, Fuda NJ, Shalloway D, Goldberg ML. Greatwall-phosphorylated Endosulfine is both an inhibitor and a substrate of PP2A-B55 heterotrimers. eLife 2014; 3:e01695; PMID:24618897; https://doi.org/10.7554/eLife.01695
   PubMed Web of Science ®Google Scholar
• Kishimoto T. Entry into mitosis: a solution to the decades-long enigma of MPF. Chromosoma 2015; 124:417-28; PMID:25712366; https://doi.org/10.1007/s00412-015-0508-y
   PubMed Web of Science ®Google Scholar
• Lindqvist A, Rodriguez-Bravo V, Medema RH. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J Cell Biol 2009; 185:193-202; PMID:19364923; https://doi.org/10.1083/jcb.200812045
   PubMed Web of Science ®Google Scholar
• Hegarat N, Rata S, Hochegger H. Bistability of mitotic entry and exit switches during open mitosis in mammalian cells. BioEssays 2016; 38:627-43; PMID:27231150; https://doi.org/10.1002/bies.201600057
   PubMed Web of Science ®Google Scholar
• Yu J, Zhao Y, Li Z, Galas S, Goldberg ML. Greatwall kinase participates in the CDC2 autoregulatory loop in Xenopus egg extracts. Mol Cell 2006; 22:83-91; PMID:16600872; https://doi.org/10.1016/j.molcel.2006.02.022
   PubMed Web of Science ®Google Scholar
• Vigneron S, Brioudes E, Burgess A, Labbe JC, Lorca T, Castro A. Greatwall maintains mitosis through regulation of PP2A. EMBO J 2009; 28(18):2786-93; PMID:19680222; https://doi.org/10.1038/emboj.2009.228
   PubMed Web of Science ®Google Scholar
• Burgess A, Vigneron S, Brioudes E, Labbe JC, Lorca T, Castro A. 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 U S A 2010; 107:12564-9; PMID:20538976; https://doi.org/10.1073/pnas.0914191107
   PubMed Web of Science ®Google Scholar
• Lorca T, Bernis C, Vigneron S, Burgess A, Brioudes E, Labbe JC, Castro A. 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 2010; 123:2281-91; PMID:20554897; https://doi.org/10.1242/jcs.064527
   PubMed Web of Science ®Google Scholar
• Schmitz MH, Held M, Janssens V, Hutchins JR, Hudecz O, Ivanova E, Goris J, Trinkle-Mulcahy L, Lamond AI, Poser I, et al. Live-cell imaging RNAi screen identifies PP2A-B55alpha and importin-beta1 as key mitotic exit regulators in human cells. Nat Cell Biol 2010; 12:886-93; PMID:20711181; https://doi.org/10.1038/ncb2092
   PubMed Web of Science ®Google Scholar
• Mochida S. Regulation of alpha-endosulfine, an inhibitor of protein phosphatase 2A, by multisite phosphorylation. FEBS J 2014; 281:1159-69; PMID:24354984; https://doi.org/10.1111/febs.12685
   PubMed Web of Science ®Google Scholar
• Dulubova I, Horiuchi A, Snyder GL, Girault JA, Czernik AJ, Shao L, Ramabhadran R, Greengard P, Nairn AC. ARPP-16/ARPP-19: a highly conserved family of cAMP-regulated phosphoproteins. J Neurochem 2001; 77:229-38; PMID:11279279; https://doi.org/10.1046/j.1471-4159.2001.t01-1-00191.x
   PubMed Web of Science ®Google Scholar
• Okumura E, Morita A, Wakai M, Mochida S, Hara M, Kishimoto T. Cyclin B-Cdk1 inhibits protein phosphatase PP2A-B55 via a Greatwall kinase-independent mechanism. J Cell Biol 2014; 204:881-9; PMID:24616226; https://doi.org/10.1083/jcb.201307160
   PubMed Web of Science ®Google Scholar
• Dupre A, Daldello EM, Nairn AC, Jessus C, Haccard O. Phosphorylation of ARPP19 by protein kinase A prevents meiosis resumption in Xenopus oocytes. Nat commun 2014; 5:3318; PMID:24525567; https://doi.org/10.1038/ncomms4318
   PubMed Web of Science ®Google Scholar
• Mulner O, Huchon D, Thibier C, Ozon R. Cyclic AMP synthesis in Xenopus laevis oocytes: inhibition by progesterone. Biochim Biophys Acta 1979; 582:179-84; PMID:83880; https://doi.org/10.1016/0304-4165(79)90301-5
   PubMed Web of Science ®Google Scholar
• Ozon R, Belle R, Huchon D, Mulner O. Roles of cyclic AMP and calcium in maturation of Xenopus laevis oocytes. J Steroid Biochem 1979; 11:709-13; PMID:226799; https://doi.org/10.1016/0022-4731(79)90004-9
   PubMedGoogle Scholar
• Ozon R, Marot J, Huchon D. Progesterone stimulated meiotic maturation in Xenopus laevis: inhibition by methylxanthines. Res Steroids 1979; 8:259-63.
   Google Scholar
• Smith LD. The induction of oocyte maturation: transmembrane signalling events and regulation of the cell cycle. Development 1989; 107:685-99; PMID:2698799
   PubMed Web of Science ®Google Scholar
• Wang J, Liu XJ. Progesterone inhibits protein kinase A (PKA) in Xenopus oocytes: demonstration of endogenous PKA activities using an expressed substrate. J Cell Sci 2004; 117:5107-16; PMID:15456849; https://doi.org/10.1242/jcs.01383
   PubMed Web of Science ®Google Scholar
• Maller JL, Butcher FR, Krebs EG. Early effect of progesterone on levels of cyclic adenosine 3′:5′- monophosphate in Xenopus oocytes. J Biol Chem 1979; 254:579-82; PMID:216678
   PubMed Web of Science ®Google Scholar
• Nader N, Courjaret R, Dib M, Kulkarni RP, Machaca K. Release from Xenopus oocyte prophase I meiotic arrest is independent of a decrease in cAMP levels or PKA activity. Development 2016; 143:1926-36; PMID:27122173; https://doi.org/10.1242/dev.136168
   PubMed Web of Science ®Google Scholar
• Maller JL, Krebs EG. Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3′:5′-monophosphate-dependent protein kinase. J Biol Chem 1977; 252:1712-8; PMID:190238
   PubMed Web of Science ®Google Scholar
• Huchon D, Ozon R, Fischer EH, Demaille JG. The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. Mol Cell Endocrinol 1981; 22:211-22; PMID:7016632; https://doi.org/10.1016/0303-7207(81)90092-7
   PubMed Web of Science ®Google Scholar
• Rime H, Haccard O, Ozon R. Activation of p34cdc2 kinase by cyclin is negatively regulated by cyclic amp-dependent protein kinase in Xenopus oocytes. Dev Biol 1992; 151:105-10; PMID:1533599; https://doi.org/10.1016/0012-1606(92)90217-5
   PubMed Web of Science ®Google Scholar
• Eyers PA, Liu J, Hayashi NR, Lewellyn AL, Gautier J, Maller JL. Regulation of the G2/M transition in Xenopus oocytes by the cAMP-dependent protein kinase. J Biol Chem 2005; 280(26):24339–46; PMID:15860459; https://doi.org/10.1074/jbc.M412442200
   PubMed Web of Science ®Google Scholar
• Matten W, Daar I, Vande Woude GF. Protein kinase A acts at multiple points to inhibit Xenopus oocyte maturation. Mol Cell Biol 1994; 14:4419-26; PMID:8007949; https://doi.org/10.1128/MCB.14.7.4419
   PubMed Web of Science ®Google Scholar
• Daar I, Yew N, Vande Woude GF. Inhibition of mos-induced oocyte maturation by protein kinase A. J Cell Biol 1993; 120:1197-202; PMID:8436591; https://doi.org/10.1083/jcb.120.5.1197
   PubMed Web of Science ®Google Scholar
• Duckworth BC, Weaver JS, Ruderman JV. G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. Proc Natl Acad Sci USA 2002; 99:16794-9; PMID:12477927; https://doi.org/10.1073/pnas.222661299
   PubMed Web of Science ®Google Scholar
• Haccard O, Jessus C. Oocyte maturation, Mos and cyclins-a matter of synthesis: two functionally redundant ways to induce meiotic maturation. Cell Cycle 2006; 5:1152-9; PMID:16760654; https://doi.org/10.4161/cc.5.11.2800
   PubMed Web of Science ®Google Scholar
• Gaffre M, Martoriati A, Belhachemi N, Chambon JP, Houliston E, Jessus C, Karaiskou A. A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes. Development 2011; 138:3735-44; PMID:21795279; https://doi.org/10.1242/dev.063974
   PubMed Web of Science ®Google Scholar
• De Smedt V, Poulhe R, Cayla X, Dessauge F, Karaiskou A, Jessus C, Ozon R. Thr-161 Phosphorylation of Monomeric Cdc2. Regulation by protein phosphatase 2C in Xenopus oocyte. J Biol Chem 2002; 277:28592-600; PMID:12036957; https://doi.org/10.1074/jbc.M202742200
   PubMed Web of Science ®Google Scholar
• Wang J, Cao WL, Liu XJ. Protein kinase A(PKA)-restrictive and PKA-permissive phases of oocyte maturation. Cell Cycle 2006; 5:213-7; PMID:16397412; https://doi.org/10.4161/cc.5.2.2365
   PubMed Web of Science ®Google Scholar
• Frank-Vaillant M, Jessus C, Ozon R, Maller JL, Haccard O. Two distinct mechanisms control the accumulation of cyclin B1 and mos in Xenopus oocytes in response to progesterone. Mol Biol Cell 1999; 10:3279-88; PMID:10512866; https://doi.org/10.1091/mbc.10.10.3279
   PubMed Web of Science ®Google Scholar
• Goris J, Hermann J, Hendrix P, Ozon R, Merlevede W. Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. FEBS Lett 1989; 245:91-4; PMID:2538367; https://doi.org/10.1016/0014-5793(89)80198-X
   PubMed Web of Science ®Google Scholar
• Huchon D, Ozon R. Effects of 3-isobutyl-methylxanthine (IBMX) and of cholera toxin on maturation induced by the injection of maturation promoting factor (MPF) in oocyte of Xenopus laevis. Biol Cell 1979; 35:15-20.
   Google Scholar
• Andrade EC, Musante V, Horiuchi A, Matsuzaki H, Brody AH, Wu T, Greengard P, Taylor JR, Nairn AC. ARPP-16 is a striatal-enriched inhibitor of protein phosphatase 2A regulated by microtubule-associated serine/threonine kinase 3 (Mast 3 kinase). J Neurosci 2017; 37:2709-22; PMID:28167675; https://doi.org/10.1523/JNEUROSCI.4559-15.2017
   PubMed Web of Science ®Google Scholar
• Bosch M, Cayla X, Van Hoof C, Hemmings BA, Ozon R, Merlevede W, Goris J. The PR55 and PR65 subunits of protein phosphatase 2A from Xenopus laevis molecular cloning and developmental regulation of expression. Eur J Biochem 1995; 230:1037-45; PMID:7601134; https://doi.org/10.1111/j.1432-1033.1995.tb20653.x
   PubMedGoogle Scholar
• Studier FW. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 2005; 41:207-34; PMID:15915565; https://doi.org/10.1016/j.pep.2005.01.016
   PubMed Web of Science ®Google Scholar
• Daldello EM, Le T, Poulhe R, Jessus C, Haccard O, Dupre A. Fine-tuning of Cdc6 accumulation by Cdk1 and MAP kinase is essential for completion of oocyte meiotic divisions. J Cell Sci 2015; 128:2482-96; PMID:26092930; https://doi.org/10.1242/jcs.166553
   PubMed Web of Science ®Google Scholar