Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity

Biology of Reproduction

Volumn 76, Issue 4, 2007, Pages 628-638

  Swain, Jason E ^a,b   Ding, Jun ^b   Brautigan, David L ^c   Villa Moruzzi, Emma ^d   Smith, Gary D ^a,b,e  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF PISA   (Italy)

^e NONE   (United States)

Author keywords

Gamete biology; Kinases; Meiosis; Oocyte development; Phosphatases

Indexed keywords

CALYCULIN A; GLYCOGEN SYNTHASE KINASE 3; HISTONE H3; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEIN PPP1R2; PROTEIN SUBUNIT; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CHROMATIN CONDENSATION; CHROMOSOME ABERRATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; FEMALE; GERMINAL VESICLE; IMMUNOCYTOCHEMISTRY; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; WESTERN BLOTTING;

ANIMALS; CHROMATIN; CHROMOSOMES, MAMMALIAN; FEMALE; HELA CELLS; HISTONES; HUMANS; MEIOSIS; MICE; MICE, INBRED STRAINS; OKADAIC ACID; OOCYTES; OXAZOLES; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTAMINE KINASE;

EID: 33947513747     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.106.055798     Document Type: Article

References (88)

1. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001; 2:280-291.
2. Hunt PA. The control of mammalian female meiosis: factors that influence chromosome segregation. J Assist Reprod Genet 1998; 15:246-252.
3. Hassold T, Hunt PA, Sherman S. Trisomy in humans: incidence, origin and etiology. Curr Opin Genet Dev 1993; 3:398-403.
4. Chan RC, Severson AF, Meyer BJ. Condensin restructures chromosomes in preparation for meiotic divisions. J Cell Biol 2004; 167:613-625.
5. Wolffe A. Chromatin Structure and Function. London: Academic Press; 1995.
6. Tanaka M, Hennebold JD, Macfarlane J, Adashi EY. A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 2001; 128:655-664.
7. Bradbury EM. Reversible histone modifications and the chromosome cell cycle. Bioessays 1992; 14:9-16.
8. Bradbury EM, Inglis RJ, Matthews HR, Sarner N. Phosphorylation of very-lysine-rich histone in Physarum polycephalum. Correlation with chromosome condensation. Eur J Biochem 1973; 33:131-139.
9. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 1999; 274:25543-25549.
10. Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci U S A 1998; 95:7480-7484.
11. Wei Y, Yu L, Bowen J, Gorovsky M, Allis C. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999; 97:99-109.
12. Houben A, Demidov D, Rutten T, Scheidtmann KH. Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells. Cytogenet Genome Res 2005; 109:148-155.
13. Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA. Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci 1998; 111:3497-3506.
14. Kaszas E, Cande WZ. Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J Cell Sci 2000; 113:3217-3226.
15. Schmitt A, Gutierrez GJ, Lenart P, Ellenberg J, Nebreda AR. Histone H3 phosphorylation during Xenopus oocyte maturation: regulation by the MAP kinase/p90Rsk pathway and uncoupling from DNA condensation. FEBS Lett 2002; 518:23-28.
16. Fuchs J, Demidov D, Houben A, Schubert I. Chromosomal histone modification patterns-from conservation to diversity. Trends Plant Sci 2006; 11:199-208.
17. Cohen P. The structure and regulation of protein phosphatases. Annu Rev Biochem 1989; 58:453-508.
18. da Cruz e Silva EF, Fox CA, Ouimet CC, Gustafson E, Watson SJ, Greengard P. Differential expression of protein phosphatase 1 isoforms in mammalian brain. J Neurosci 1995; 15:3375-3389.
19. Tognarini M, Villa-Moruzzi E. Analysis of the isoforms of protein phosphatase 1 (PP1) with polyclonal peptide antibodies. Methods Mol Biol 1998; 93:169-183.
20. Zhang ZJ, Bai G, Shima M, Zhao SM, Nagao M, Lee EY. Expression and characterization of rat protein phosphatases-1 alpha, -1 gamma 1, -1 gamma 2, and -1 delta. Arch Biochem Biophys 1993; 303:402-406.
21. Sasaki K, Shima H, Kitagawa Y, Irino S, Sugimura T, Nagao M. Identification of members of the protein phosphatase 1 gene family in the rat and enhanced expression of protein phosphatase 1 alpha gene in rat hepatocellular carcinomas. Jpn J Cancer Res 1990; 81:1272-1280.
22. Smith GD, Sadhu A, Mathies S, Wolf DP. Characterization of protein phosphatases in mouse oocytes. Dev Biol 1998; 204:537-549.
23. Swain JE, Wang X, Saunders TL, Dunn RL, Smith GD. Specific inhibition of mouse oocyte nuclear protein phosphatase-1 stimulates germinal vesicle breakdown. Mol Reprod Dev 2003; 65:96-103.
24. Bialojan C, Takai A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 1988; 256:283-290.
25. Gavin AC, 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; 192:75-81.
26. Rime H, Ozon R. Protein phosphatases are involved in the in vivo activation of histone H1 kinase in mouse oocyte. Dev Biol 1990; 141:115-122.
27. Smith GD, Sadhu A, Wolf DP. Transient exposure of rhesus macaque oocytes to calyculin-A and okadaic acid stimulates germinal vesicle breakdown permitting subsequent development and fertilization. Biol Reprod 1998; 58:880-886.
28. Wang X, Swain JE, Bollen M, Liu XT, Ohl DA, Smith GD. Endogenous regulators of protein phosphatase-1 during mouse oocyte development and meiosis. Reproduction 2004; 128:493-502.
29. Ingebritsen T, Stewart A, Cohen A. The protein phosphatases involved in cellular regulation. 6. Measurement of type-1 and type-2 protein phosphatases in extracts of mammalian tissues; an assessment of their physiological roles. Eur J Biochem 1983; 132:297-307.
30. Endo S, Zhou X, Connor J, Wang B, Shenoliker S. Multiple structural elements define the specificity of recombinant human inhibitor-1 as a protein phosphatase-1 inhibitor. Biochemistry 1996; 35:5220-5228.
31. DePaoli-Roach AA. Synergistic phosphorylation and activation of ATP-Mg-dependent phosphoprotein phosphatase by F A/GSK-3 and casein kinase II (PC0.7). J Biol Chem 1984; 259:12144-12152.
32. Hemmings BA, Resink TJ, Cohen P. Reconstitution of a Mg-ATP-dependent protein phosphatase and its activation through a phosphorylation mechanism. FEBS Lett 1982; 150:319-324.
33. Yang SD, Vandenheede JR, Merlevede W. Identification of inhibitor-2 as the ATP-mg-dependent protein phosphatase modulator. J Biol Chem 1981; 256:10231-10234.
34. Puntoni F, Villa-Moruzzi E. Phosphorylation of the inhibitor-2 of protein phosphatase-1 by cdc2-cyclin B and GSK3. Biochem Biophys Res Commun 1995; 207:732-739.
35. Sakashita G, Shima H, Komatsu M, Urano T, Kikuchi A, Kikuchi K. Regulation of type 1 protein phosphatase/inhibitor-2 complex by glycogen synthase kinase-3beta in intact cells. J Biochem (Tokyo) 2003; 133:165-171.
36. Hodges C, Hunt P. Simultaneous analysis of chromosomes and chromosome-associated proteins in mammalian oocytes and embryos. Chromosoma 2002; 111:165-169.
37. Andreassen P, Lacroix F, Villa-Moruzzi E, Margolis R. Differential subcellular localization of protein phosphatase-1 alpha, gamma 1, and delta isoforms during both interphase and mitosis in mammalian cells. J Cell Biol 1998; 141:1207-1215.
38. Boonstra J, Verkleij AJ. Regulation of enzyme activity in vivo is determined by its cellular localization. Adv Enzyme Regul 2004; 44:61-73.
39. Lu Q, Dunn RL, Angeles R, Smith GD. Regulation of spindle formation by active mitogen-activated protein kinase and protein phosphatase 2A during mouse oocyte meiosis. Biol Reprod 2002; 66:29-37.
40. Wang X, Liu X, Dunn RL, Ohl DA, Smith GD. Glycogen synthase kinase-3 regulates mouse oocyte homologue segregation. Mol Reprod Dev 2003; 64:96-105.
41. Mailhes JB, Hilliard C, Fuseler JW, London SN. 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; 11:619-631.
42. Alexandre H, Van Cauwenberge A, Tsukitani Y, Mulnard J. Pleiotropic effect of okadaic acid on maturing mouse oocytes. Development 1991; 112:971-980.
43. Brunet S, Maro B. 2005 Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005; 130:801-811.
44. Compton DA. Spindle assembly in animal cells. Annu Rev Biochem 2000; 69:95-114.
45. Hirano T. Chromosome cohesion, condensation, and separation. Annu Rev Biochem 2000; 69:115-144.
46. Schmiesing JA, Gregson HC, Zhou S, Yokomori K. A human condensin complex containing hCAP-C-hCAP-E and CNAP1, a homolog of Xenopus XCAP-D2, colocalizes with phosphorylated histone H3 during the early stage of mitotic chromosome condensation. Mol Cell Biol 2000; 20:6996-7006.
47. Ball AR Jr, Schmiesing JA, Zhou C, Gregson HC, Okada Y, Doi T, Yokomori K. Identification of a chromosome-targeting domain in the human condensin subunit CNAP1/hCAP-D2/Eg7. Mol Cell Biol 2002; 22:5769-5781.
48. Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM. Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 2004; 117:6435-6445.
49. Ono T, Fang Y, Spector DL, Hirano T. Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 2004; 15:3296-3308.
50. Mattson BA, Albertini DF. Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev 1990; 25:374-383.
51. Motlik J, Fulka J. Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. J Exp Zool 1976; 198:155-162.
52. Bui HT, 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; 70:1843-1851.
53. Jelinkova L, Kubelka M. Neither Aurora B activity nor histone H3 phosphorylation is essential for chromosome condensation curing meiotic maturation of porcine oocytes. Biol Reprod 2006; 74:905-912.
54. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, Bishop D, Grushcow JM, Brame CJ, Caldwell JA, Hunt DE, Lin R, Smith MM, et al. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and GLC7/PP1 phosphatase in budding yeast and nematodes. Cell 2000; 102:279-291.
55. Bezrookove V, Smits R, Moeslein G, Fodde R, Tanke HJ, Raap AK, Darroudi F. Premature chromosome condensation revisited: a novel chemical approach permits efficient cytogenetic analysis of cancers. Genes Chromosomes Cancer 2003; 38:177-186.
56. Terzoudi GI, Malik SI, Pantelias GE, Margaritis K, Manola K, Makropoulos W. A new cytogenetic approach for the evaluation of mutagenic potential of chemicals that induce cell cycle arrest in the G2 phase. Mutagenesis 2003; 18:539-543.
57. Shima H, Haneji T, Hatano Y, Kasugai I, Sugimura T, Nagao M. Protein phosphatase 1 gamma 2 is associated with nuclei of meiotic cells in rat testis. Biochem Biophys Res Commun 1993; 194:930-937.
58. Smith GD, Wolf DP, Trautman KC, da Cruz e Silva EF, Greengard P, Vijayaraghavan S. Primate sperm contain protein phosphatase 1, a biochemical mediator of motility. Biol Reprod 1996; 54:719-727.
59. Dombradi V, Axton JM, Barker HM, Cohen PT. Protein phosphatase 1 activity in Drosophila mutants with abnormalities in mitosis and chromosome condensation. FEBS Lett 1990; 275:39-43.
60. Dombradi V, Cohen PT. Protein phosphorylation is involved in the regulation of chromatin condensation during interphase. FEBS Lett 1992; 312:21-26.
61. Mills J, Lee VM, Pittman RN. Activation of a PP2A-like phosphatase and dephosphorylation of tau protein characterize onset of the execution phase of apoptosis. J Cell Sci 1998; 111:625-636.
62. Sontag E, Nunbhakdi-Craig V, Lee G, Bloom G, Mumby M. Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron 1996; 17:1201-1207.
63. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White CI, Mumby M, Bloom G. Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 1999; 274:25490-25498.
64. Favre B, Turowski P, Hemmings BA. Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J Biol Chem 1997; 272:13856-13863.
65. Turowski P, Fernandez A, Favre B, Lamb NJ, Hemmings BA. Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression. J Cell Biol 1995; 129:397-410.
66. Murnion M, Adams R, Callister D, Allis C, Earnshaw W, Swedlow J. Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J Biol Chem 2001; 276:26656-26665.
67. Goto H, Yasui Y, Nigg EA, Inagaki M. Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 2002; 7:11-17.
68. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, Sen S, Allis CD, Sassone-Corsi P. Mitotic phosphorylation of histone H3: spatiotemporal regulation by mammalian Aurora kinases. Mol Cell Biol 2002; 22:874-885.
69. Yao LJ, Zhong ZS, Zhang LS, Chen DY, Schatten H, Sun QY. Aurora-A is a critical regulator of microtubule assembly and nuclear activity in mouse oocytes, fertilized eggs, and early embryos. Biol Reprod 2004; 70:1392-1399.
70. Yao LJ, Sun QY. Characterization of aurora-a in porcine oocytes and early embryos implies its functional roles in the regulation of meiotic maturation, fertilization and cleavage. Zygote 2005; 13:23-30.
71. Satinover DL, Leach CA, Stukenberg PT, Brautigan DL. Activation of Aurora-A kinase by protein phosphatase inhibitor-2, a bifunctional signaling protein. Proc Natl Acad Sci U S A 2004; 101:8625-8630.
72. Glover DM, Leibowitz MH, McLean DA, Parry H. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 1995; 81:95-105.
73. Huang FL, Glinsmann WH. Separation and characterization of two phosphorylase phosphatase inhibitors from rabbit skeletal muscle. Eur J Biochem 1976; 70:419-426.
74. Brautigan DL, Sunwoo J, Labbe JC, Fernandez A, Lamb NJ. Cell cycle oscillation of phosphatase inhibitor-2 in rat fibroblasts coincident with p34cdc2 restriction. Nature 1990; 344:74-78.
75. Leach C, Eto M, Brautigan DL. Domains of type 1 protein phosphatase inhibitor-2 required for nuclear and cytoplasmic localization in response to cell-cell contact. J Cell Sci 2002; 115:3739-3745.
76. Tung HYL, Wang W, Chan CSM. Regulation of chromosome segregation by Glc8p, a structrual homolog of mammlian inhibitor 2 that functions as both an activator and an inhibitor of yeast protein phosphatase 1. Mol Cell Biol 1995; 15:6064-6074.
77. Pinsky BA, Kotwaliwale CV, Tatsutani SY, Breed CA, Biggins S. Glc7/protein phosphatase 1 regulatory subunits can oppose the Ipl1/aurora protein kinase by redistributing Glc7. Mol Cell Biol 2006; 26:2648-2660.
78. Osawa Y, Nakagama H, Shima H, Sugimura T, Nagao M. Identification and characterization of three isotypes of protein phosphatase inhibitor-2 and their expression profiles during testis maturation in rats. Eur J Biochem 1996; 242:793-798.
79. Acevedo N, Wang X, Dunn RL, Smith GD. Glycogen synthase kinase-3 regulation of chromatin segregation and cytokinesis in mouse preimplantation embryos. Mol Reprod Dev 2007; 74:178-188.
80. Leost M, Schultz C, Link A, Wu YZ, Biernat J, Mandelkow EM, Bibb JA, Snyder GL, Greengard P, Zaharevitz DW, Gussio R, Senderowicz AM, et al. Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25. Eur J Biochem 2000; 267:5983-5994.
81. Tatebayashi Y, Haque N, Tung YC, Iqbal K, Grundke-Iqbal I. Role of tau phosphorylation by glycogen synthase kinase-3beta in the regulation of organelle transport. J Cell Sci 2004; 117:1653-1663.
82. Leach C, Shenolikar S, Brautigan DL. Phosphorylation of phosphatase inhibitor-2 at centrosomes during mitosis. J Biol Chem 2003; 278:26015-26020.
83. Li M, Stefansson B, Wang W, Schaefer EM, Brautigan DL. Phosphorylation of the Pro-X-Thr-Pro site in phosphatase inhibitor-2 by cyclin-dependent protein kinase during M-phase of the cell cycle. Cell Signal 2006; 18:1318-1326.
84. Marchal R, Tomanek M, Terqui M, Mermillod P. Effects of cell cycle dependent kinases inhibitor on nuclear and cytoplasmic maturation of porcine oocytes. Mol Reprod Dev 2001; 60:65-73.
85. Mermillod P, Tomanek M, Marchal R, Meijer L. High developmental competence of cattle oocytes maintained at germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Mol Reprod Dev 2000; 55:89-95.
86. Kubelka M, Anger M, Kalous J, Schultz RM, Motlik J. Chromosome condensation in pig oocytes: lack of a requirement for either cdc2 kinase or MAP kinase activity. Mol Reprod Dev 2002; 63:110-118.
87. Kubelka M, Motlik J, Schultz RM, Pavlok A. Butyrolactone I reversibly inhibits meiotic maturation of bovine oocytes, without influencing chromosome condensation activity. Biol Reprod 2000; 62:292-302.
88. Eto M, Elliott E, Prickett TD, Brautigan DL. Inhibitor-2 regulates protein phosphatase-1 complexed with NimA-related kinase to induce centrosome separation. J Biol Chem 2002; 277:44013-44020.