Oscillations in PP1 activity are essential for accurate progression through mammalian oocyte meiosis

References

• Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet. 2001;2(4):280–291. doi: 10.1038/35066065
   PubMed Web of Science ®Google Scholar
• Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet. 2012;13(7):493–504. doi: 10.1038/nrg3245
   PubMed Web of Science ®Google Scholar
• Crncec A, Hochegger H. Triggering mitosis. FEBS Lett. 2019;593(20):2868–2888. doi: 10.1002/1873-3468.13635
   PubMed Web of Science ®Google Scholar
• Adhikari D, Zheng W, Shen Y, et al. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum Mol Genet. 2012;21(11):2476–2484. doi: 10.1093/hmg/dds061
   PubMed Web of Science ®Google Scholar
• St-Denis N, Gupta GD, Lin ZY, et al. Phenotypic and interaction profiling of the human phosphatases identifies diverse mitotic regulators. Cell Rep. 2016;17(9):2488–2501. doi: 10.1016/j.celrep.2016.10.078
   PubMed Web of Science ®Google Scholar
• Bancroft J, Holder J, Geraghty Z, et al. PP1 promotes cyclin B destruction and the metaphase–anaphase transition by dephosphorylating CDC20. Mol Biol Cell. 2020;31(21):2315–2330. doi: 10.1091/mbc.E20-04-0252
   PubMed Web of Science ®Google Scholar
• Rogers S, Fey D, McCloy RA, et al. PP1 initiates the dephosphorylation of MASTL, triggering mitotic exit and bistability in human cells. J Cell Sci. 2016;129:1340. doi: 10.1242/jcs.179754
   PubMed Web of Science ®Google Scholar
• Ma S, Vigneron S, Robert P, et al. Greatwall dephosphorylation and inactivation upon mitotic exit is triggered by PP1. J Cell Sci. 2016;129:1329. doi: 10.1242/jcs.178855
   PubMed Web of Science ®Google Scholar
• Grallert A, Boke E, Hagting A, et al. A PP1–PP2A phosphatase relay controls mitotic progression. Nature. 2015;517(7532):94–98. doi: 10.1038/nature14019
   PubMed Web of Science ®Google Scholar
• Tang A, Shi P, Song A, et al. PP2A regulates kinetochore-microtubule attachment during meiosis I in oocyte. Cell Cycle. 2016;15(11):1450–1461. doi: 10.1080/15384101.2016.1175256
   PubMed Web of Science ®Google Scholar
• Hu M-W, Wang Z-B, Jiang Z-Z, et al. Scaffold subunit Aalpha of PP2A is essential for female meiosis and fertility in mice. Biol Reprod. 2014;91(1):19. doi: 10.1095/biolreprod.114.120220
   PubMed Web of Science ®Google Scholar
• Alexandre H, Van Cauwenberge A, Tsukitani Y, et al. Pleiotropic effect of okadaic acid on maturing mouse oocytes. Development. 1991;112(4):971–980. doi: 10.1242/dev.112.4.971
   PubMed Web of Science ®Google Scholar
• Schwartz DA, Schultz RM. 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 Biology. 1991;145(1):119–127. doi: 10.1016/0012-1606(91)90218-R
   PubMed Web of Science ®Google Scholar
• Mailhes JB, Hilliard C, Fuseler JW, et al. 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. 2003;11(6):619–631. doi: 10.1023/A:1024909119593
   PubMed Web of Science ®Google Scholar
• Gavin A-C, Tsukitani Y, Schorderet-Slatkine S. Induction of M-phase entry of prophase-blocked mouse oocytes through microinjection of okadaic acid, a specific phosphatase inhibitor. Exp Cell Res. 1991;192(1):75–81. doi:10.1016/0014-4827(91)90159-R
   PubMed Web of Science ®Google Scholar
• Smith GD, Sadhu A, Mathies S, et al. Characterization of protein phosphatases in mouse oocytes. Dev Biology. 1998;204(2):537–549. doi: 10.1006/dbio.1998.9043
   PubMed Web of Science ®Google Scholar
• Swain JE, Wang X, Saunders TL, et al. Specific inhibition of mouse oocyte nuclear protein phosphatase-1 stimulates germinal vesicle breakdown. Mol Reprod Dev. 2003;65(1):96–103. doi: 10.1002/mrd.10258
   PubMed Web of Science ®Google Scholar
• Swain JE, Ding J, Brautigan DL, et al. Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity. Biol Reprod. 2007;76(4):628–638. doi: 10.1095/biolreprod.106.055798
   PubMed Web of Science ®Google Scholar
• Wang X, Swain JE, Bollen M, et al. Endogenous regulators of protein phosphatase-1 during mouse oocyte development and meiosis. Reproduction. 2004;128(5):493–502. doi: 10.1530/rep.1.00173
   PubMed Web of Science ®Google Scholar
• Wang L-I, Das A, McKim KS, et al. Sister centromere fusion during meiosis I depends on maintaining cohesins and destabilizing microtubule attachments. PLoS Genet. 2019;15(5):e1008072. doi: 10.1371/journal.pgen.1008072
   PubMed Web of Science ®Google Scholar
• Hattersley N, Cheerambathur D, Moyle M, et al. A nucleoporin docks protein phosphatase 1 to direct meiotic chromosome segregation and nuclear assembly. Dev Cell. 2016;38(5):463–477. doi: 10.1016/j.devcel.2016.08.006
   PubMed Web of Science ®Google Scholar
• Oppedisano L, Haines G, Hrabchak C, et al. The rate of aneuploidy is altered in spermatids from infertile mice. Hum Reprod. 2002;17(3):710–717. doi: 10.1093/humrep/17.3.710
   PubMed Web of Science ®Google Scholar
• Swartz SZ, Nguyen HT, McEwan BC, et al. Selective dephosphorylation by PP2A-B55 directs the meiosis I-meiosis II transition in oocytes. Elife. 2021;10:e70588. doi: 10.7554/eLife.70588
   PubMed Web of Science ®Google Scholar
• Bollen M, Peti W, Ragusa MJ, et al. The extended PP1 toolkit: designed to create specificity. Trends Biochem Sci. 2010;35(8):450–458. doi: 10.1016/j.tibs.2010.03.002
   PubMed Web of Science ®Google Scholar
• Heroes E, Lesage B, Görnemann J, et al. The PP1 binding code: a molecular-lego strategy that governs specificity. FEBS J. 2013;280(2):584–595. doi: 10.1111/j.1742-4658.2012.08547.x
   PubMed Web of Science ®Google Scholar
• Winkler C, De Munter S, Van Dessel N, et al. The selective inhibition of protein phosphatase-1 results in mitotic catastrophe and impaired tumor growth. J Cell Sci. 2015;128:4526. doi: 10.1242/jcs.175588
   PubMed Web of Science ®Google Scholar
• Bhowmick R, Thakur RS, Venegas AB, et al. The RIF1-PP1 axis controls abscission timing in human cells. Curr Biol. 2019;29(7):1232–42.e5. doi: 10.1016/j.cub.2019.02.037
   PubMed Web of Science ®Google Scholar
• Cheng A, Dean NM, Honkanen RE. Serine/Threonine protein phosphatase type 1γ1 is required for the completion of cytokinesis in human A549 lung carcinoma cells. J Biol Chem. 2000;275(3):1846–1854. doi: 10.1074/jbc.275.3.1846
   PubMed Web of Science ®Google Scholar
• Capalbo L, Bassi ZI, Geymonat M, et al. The midbody interactome reveals unexpected roles for PP1 phosphatases in cytokinesis. Nat Commun. 2019;10(1):4513. doi: 10.1038/s41467-019-12507-9
   PubMed Web of Science ®Google Scholar
• Conti D, Gul P, Islam A, et al. Kinetochores attached to microtubule-ends are stabilised by Astrin bound PP1 to ensure proper chromosome segregation. Elife. 2019;8:e49325. doi: 10.7554/eLife.49325
   PubMed Web of Science ®Google Scholar
• Margolis SS, Walsh S, Weiser DC, et al. PP1 control of M phase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation. Embo J. 2003;22(21):5734–5745. doi: 10.1093/emboj/cdg545
   PubMed Web of Science ®Google Scholar
• Smith RJ, Cordeiro MH, Davey NE, et al. PP1 and PP2A use opposite phospho-dependencies to control distinct processes at the kinetochore. Cell Rep. 2019;28(8):2206–19.e8. doi: 10.1016/j.celrep.2019.07.067
   PubMed Web of Science ®Google Scholar
• Nasa I, Rusin SF, Kettenbach AN, et al. Aurora B opposes PP1 function in mitosis by phosphorylating the conserved PP1-binding RVxF motif in PP1 regulatory proteins. Sci Signaling. 2018;11(530):11. doi: 10.1126/scisignal.aai8669
   Web of Science ®Google Scholar
• Kwon YG, Lee SY, Choi Y, et al. Cell cycle-dependent phosphorylation of mammalian protein phosphatase 1 by cdc2 kinase. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94:2168–2173.
   PubMed Web of Science ®Google Scholar
• Dohadwala M, da Cruze Silva EF, Hall FL, et al. Phosphorylation and inactivation of protein phosphatase 1 by cyclin-dependent kinases. Proc Natl Acad Sci USA. 1994; 91:6408–6412 doi: 10.1073/pnas.91.14.6408.
   PubMed Web of Science ®Google Scholar
• Mitsuhashi S, Matsuura N, Ubukata M, et al. Tautomycetin is a novel and specific inhibitor of serine/threonine protein phosphatase type 1, PP1. Biochem Biophys Res Commun. 2001;287(2):328–331. doi: 10.1006/bbrc.2001.5596
   PubMed Web of Science ®Google Scholar
• Wang Y, Hoermann B, Pavic K, et al. Interrogating PP1 activity in the MAPK pathway with optimized PP1-disrupting peptides. Chembiochem. 2019;20(1):66–71. doi: 10.1002/cbic.201800541
   PubMed Web of Science ®Google Scholar
• Kalous J, Solc P, Baran V, et al. PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol Cell. 2006;98(2):111–123. doi: 10.1042/BC20050020
   PubMed Web of Science ®Google Scholar
• Fabritius AS, Ellefson ML, McNally FJ. Nuclear and spindle positioning during oocyte meiosis. Curr Opinion Cell Biol. 2011;23(1):78–84. doi: 10.1016/j.ceb.2010.07.008
   PubMed Web of Science ®Google Scholar
• Mitsuhashi S, Shima H, Tanuma N, et al. Usage of tautomycetin, a novel inhibitor of protein phosphatase 1 (PP1), reveals that PP1 is a positive regulator of Raf-1 in vivo. J Biol Chem. 2003;278(1):82–88. doi: 10.1074/jbc.M208888200
   PubMed Web of Science ®Google Scholar
• Nguyen AL, Gentilello AS, Balboula AZ, et al. Phosphorylation of threonine 3 on histone H3 by haspin kinase is required for meiosis I in mouse oocytes. J Cell Sci. 2014;127:5066–5078. doi: 10.1242/jcs.158840
   PubMed Web of Science ®Google Scholar
• Wang Q, Wei H, Du J, et al. H3 Thr3 phosphorylation is crucial for meiotic resumption and anaphase onset in oocyte meiosis. Cell Cycle (Georgetown, Tex). 2016;15(2):213–224. doi: 10.1080/15384101.2015.1121330
   PubMed Web of Science ®Google Scholar
• Han SJ, Vaccari S, Nedachi T, et al. Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. Embo J. 2006;25(24):5716–5725. doi: 10.1038/sj.emboj.7601431
   PubMed Web of Science ®Google Scholar
• Reither G, Chatterjee J, Beullens M, et al. Chemical activators of protein phosphatase-1 induce calcium release inside intact cells. Chem Biol. 2013;20(9):1179–1186. doi: 10.1016/j.chembiol.2013.07.008
   PubMedGoogle Scholar
• Beullens M, Vulsteke V, Van Eynde A, et al. The C-terminus of NIPP1 (nuclear inhibitor of protein phosphatase-1) contains a novel binding site for protein phosphatase-1 that is controlled by tyrosine phosphorylation and RNA binding. Biochem J. 2000;352(Pt 3):651–658. doi: 10.1042/bj3520651
   PubMedGoogle Scholar
• Chatterjee J, Beullens M, Sukackaite R, et al. Development of a peptide that selectively activates protein phosphatase‐1 in living cells. Angewandte Chemie. 2012;51(40):10054–10059. doi: 10.1002/anie.201204308
   Google Scholar
• Moura M, Conde C. Phosphatases in mitosis: roles and regulation. Biomolecules. 2019;9(2):55. doi: 10.3390/biom9020055
   PubMed Web of Science ®Google Scholar
• Stein P, Schindler K. Mouse oocyte microinjection, maturation and ploidy assessment. J Vis Exp. 2011;53:2851. doi: 10.3791/2851-v
   PubMed Web of Science ®Google Scholar
• Tsafriri A, Chun S-Y, Zhang R, et al. Oocyte maturation involves compartmentalization and opposing changes of camp levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev Biology. 1996;178(2):393–402. doi: 10.1006/dbio.1996.0226
   PubMed Web of Science ®Google Scholar
• Zuccotti M, Ponce RH, Boiani M, et al. The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote. 2002;10(1):73–78. doi: 10.1017/S0967199402002101
   PubMed Web of Science ®Google Scholar
• Bellone M, Zuccotti M, Redi CA, et al. The position of the germinal vesicle and the chromatin organization together provide a marker of the developmental competence of mouse antral oocytes. Reproduction. 2009;138(4):639–643. doi: 10.1530/REP-09-0230
   PubMed Web of Science ®Google Scholar
• Vallardi G, Cordeiro MH, Saurin AT. A kinase-phosphatase network that regulates kinetochore-microtubule attachments and the SAC. In: Black B, editor Centromeres and kinetochores: discovering the molecular mechanisms underlying chromosome inheritance. Springer Cham; 2017. pp. 457–484 978-3-319-58592-5 .
   Google Scholar
• Carmody LC, Baucum AJ 2nd, Bass MA, et al. Selective targeting of the γ1 isoform of protein phosphatase 1 to F-actin in intact cells requires multiple domains in spinophilin and neurabin. FASEB J. 2008;22(6):1660–1671. doi: 10.1096/fj.07-092841
   PubMed Web of Science ®Google Scholar
• Canals D, Roddy P, Hannun YA. Protein phosphatase 1α mediates ceramide-induced erm protein dephosphorylation: a novel mechanism independent of phosphatidylinositol 4, 5-biphosphate (PIP2) and myosin/ERM phosphatase. J Biol Chem. 2012;287(13):10145–10155. doi: 10.1074/jbc.M111.306456
   PubMed Web of Science ®Google Scholar
• Vallée B, Cuberos H, Doudeau M, et al. LIMK2-1, a new isoform of human LIMK2, regulates actin cytoskeleton remodeling via a different signaling pathway than that of its two homologs, LIMK2a and LIMK2b. Biochem J. 2018;475(23):3745–3761. doi: 10.1042/BCJ20170961
   PubMedGoogle Scholar
• Evans JP, Robinson DN. The spatial and mechanical challenges of female meiosis. Mol Reprod Dev. 2011;78(10–11):769–777. doi: 10.1002/mrd.21358
   PubMed Web of Science ®Google Scholar
• Uraji J, Scheffler K, Schuh M. Functions of actin in mouse oocytes at a glance. J Cell Sci. 2018;131(22):131. doi:10.1242/jcs.218099
   Web of Science ®Google Scholar
• Gil RS, Vagnarelli P. Protein phosphatases in chromatin structure and function. Biochim Biophys Acta, Mol Cell Res. 2019;1866(1):90–101. doi: 10.1016/j.bbamcr.2018.07.016
   PubMed Web of Science ®Google Scholar
• Bui H-T, Yamaoka E, Miyano T. Involvement of histone H3 (Ser10) phosphorylation in chromosome condensation without Cdc2 kinase and mitogen-activated protein kinase activation in pig oocytes. Biol Reprod. 2004;70(6):1843–1851. doi: 10.1095/biolreprod.103.026070
   PubMed Web of Science ®Google Scholar
• Bogolyubova I, Bogolyubov D. Heterochromatin morphodynamics in late oogenesis and early embryogenesis of mammals. Cells. 2020;9(6):1497. doi: 10.3390/cells9061497
   PubMed Web of Science ®Google Scholar
• de Castro IJ, Budzak J, Di Giacinto ML, et al. Repo-man/PP1 regulates heterochromatin formation in interphase. Nat Commun. 2017;8(1):14048. doi: 10.1038/ncomms14048
   PubMedGoogle Scholar
• Hirota T, Lipp JJ, Toh B-H, et al. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature. 2005;438(7071):1176–1180. doi: 10.1038/nature04254
   PubMed Web of Science ®Google Scholar
• Fischle W, Tseng BS, Dormann HL, et al. Regulation of HP1–chromatin binding by histone H3 methylation and phosphorylation. Nature. 2005;438(7071):1116–1122. doi:10.1038/nature04219
   PubMed Web of Science ®Google Scholar
• Piskadlo E, Tavares A, Oliveira RA. Metaphase chromosome structure is dynamically maintained by condensin I-directed DNA (de)catenation. Elife. 2017;6:e26120. doi: 10.7554/eLife.26120
   PubMed Web of Science ®Google Scholar
• Hirota T, Gerlich D, Koch B, et al. Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci. 2004;117(26):6435–6445. doi: 10.1242/jcs.01604
   PubMed Web of Science ®Google Scholar
• Qian J, Lesage B, Beullens M, et al. PP1/Repo-man dephosphorylates mitotic histone H3 at T3 and regulates chromosomal aurora B targeting. Curr Biol. 2011;21(9):766–773. doi: 10.1016/j.cub.2011.03.047
   PubMed Web of Science ®Google Scholar
• Balboula AZ, Schindler K, Ohkura H. Selective disruption of aurora C kinase reveals distinct functions from auroraB kinase during meiosis in mouse oocytes. PLoS Genet. 2014;10(2):e1004194. doi: 10.1371/journal.pgen.1004194
   PubMed Web of Science ®Google Scholar
• Giet R, Glover DM. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Bio. 2001;152(4):669–682. doi: 10.1083/jcb.152.4.669
   PubMed Web of Science ®Google Scholar
• Lee J, Ogushi S, Saitou M, et al. Condensins I and II are essential for construction of bivalent chromosomes in mouse oocytes?. Mol Biol Cell. 2011;22(18):3465–3477. doi: 10.1091/mbc.e11-05-0423
   PubMed Web of Science ®Google Scholar
• Olsen JV, Vermeulen M, Santamaria A, et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signaling. 2010;3(104):ra3–ra. doi: 10.1126/scisignal.2000475
   PubMed Web of Science ®Google Scholar
• Gallego M, Kang H, Virshup DM. Protein phosphatase 1 regulates the stability of the circadian protein PER2. Biochem J. 2006;399(1):169–175. doi: 10.1042/BJ20060678
   PubMedGoogle Scholar
• Dingar D, Tu WB, Resetca D, et al. MYC dephosphorylation by the PP1/PNUTS phosphatase complex regulates chromatin binding and protein stability. Nat Commun. 2018;9(1):3502. doi: 10.1038/s41467-018-05660-0
   PubMedGoogle Scholar
• Kim T, Lara-Gonzalez P, Prevo B, et al. Kinetochores accelerate or delay APC/C activation by directing Cdc20 to opposing fates. Genes Dev. 2017;31(11):1089–1094. doi: 10.1101/gad.302067.117
   PubMed Web of Science ®Google Scholar
• Thomas C, Wetherall B, Levasseur MD, et al. A prometaphase mechanism of securin destruction is essential for meiotic progression in mouse oocytes. Nat Commun. 2021;12(1):4322. doi: 10.1038/s41467-021-24554-2
   PubMed Web of Science ®Google Scholar
• Levasseur MD, Thomas C, Davies OR, et al. Aneuploidy in oocytes is prevented by sustained CDK1 activity through degron masking in cyclin B1. Dev Cell. 2019;48(5):672–684. doi: 10.1016/j.devcel.2019.01.008
   PubMed Web of Science ®Google Scholar
• Xu P, Raetz EA, Kitagawa M, et al. BUBR1 recruits PP2A via the B56 family of targeting subunits to promote chromosome congression. Biol Open. 2013;2(5):479–486. doi: 10.1242/bio.20134051
   PubMed Web of Science ®Google Scholar
• Nijenhuis W, Vallardi G, Teixeira A, et al. Negative feedback at kinetochores underlies a responsive spindle checkpoint signal. Nat Cell Biol. 2014;16(12):1257–1264. doi: 10.1038/ncb3065
   PubMed Web of Science ®Google Scholar
• Liu D, Vleugel M, Backer CB, et al. Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J Cell Bio. 2010;188(6):809–820. doi: 10.1083/jcb.201001006
   PubMed Web of Science ®Google Scholar
• Lemonnier T, Dupré A, Jessus C. The G2-to-M transition from a phosphatase perspective: a new vision of the meiotic division. Cell Div. 2020;15(1):9. doi: 10.1186/s13008-020-00065-2
   PubMed Web of Science ®Google Scholar
• Li J, Qian WP, Sun QY. Cyclins regulating oocyte meiotic cell cycle progression. Biol Reprod. 2019;101(5):878–881. doi: 10.1093/biolre/ioz143
   PubMed Web of Science ®Google Scholar
• Kishimoto T. MPF-based meiotic cell cycle control: half a century of lessons from starfish oocytes. Proc Jpn Acad Ser B Phys Biol Sci. 2018;94(4):180–203. doi: 10.2183/pjab.94.013
   PubMed Web of Science ®Google Scholar