Histone modifications during mammalian oocyte maturation: Dynamics, regulation and functions

Cell Cycle

Volumn 9, Issue 10, 2010, Pages 1942-1950

  Gu, Ling ^a,b   Wang, Qiang ^a,b   Sun, Qing Yuan ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromatin; Histone modifications; Meiosis; Mouse; Oocyte

Indexed keywords

HISTONE H3; HISTONE H4;

ACETYLATION; CELL AGING; CELL CYCLE REGULATION; CHROMATIN; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; COW; FEMALE; GENOMIC INSTABILITY; MAMMAL; MEIOSIS; METHYLATION; MOUSE; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; SHEEP; SWINE;

MAMMALIA;

EID: 77953647707     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.10.11599     Document Type: Review

References (103)

1. Allfrey VG, Faulkner R, Mirsky AE. Acetylation and Methylation of Histones and Their Possible Role in the Regulation of Rna Synthesis. Proc Natl Acad Sci USA 1964; 51:786-94.
2. Gutierrez RM, Hnilica LS. Tissue specificity of histone phosphorylation. Science 1967; 157:1324-5.
3. Huletsky A, Niedergang C, Frechette A, Aubin R, Gaudreau A, Poirier GG. Sequential ADP-ribosylation pattern of nucleosomal histones. ADP-ribosylation of nucleosomal histones. Eur J Biochem 1985; 146:277-85.
4. Nathan D, Ingvarsdottir K, Sterner DE, Bylebyl GR, Dokmanovic M, Dorsey JA, et al. Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev 2006; 20:966-76.
5. Xu D, Bai J, Duan Q, Costa M, Dai W. Covalent modifications of histones during mitosis and meiosis. Cell Cycle 2009; 8:3688-94.
6. Rada-Iglesias A, Enroth S, Andersson R, Wanders A, Pahlman L, Komorowski J, et al. Histone H3 lysine 27 trimethylation in adult differentiated colon associated to cancer DNA hypermethylation. Epigenetics 2009; 4:107-13.
7. Koprinarova MA, Russev GC. Dynamics of histone H4 acetylation during the cell cycle. Cell Cycle 2008; 7:414-6.
8. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705.
9. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403:41-5.
10. Bloushtain-Qimron N, Yao J, Shipitsin M, Maruyama R, Polyak K. Epigenetic patterns of embryonic and adult stem cells. Cell Cycle 2009; 8:809-17.
11. Wang N, Tilly JL. Epigenetic status determines germ cell meiotic commitment in embryonic and postnatal mammalian gonads. Cell Cycle 9:339-49.
12. Fan HY, Sun QY. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 2004; 70:535-47.
13. Motlik J, Fulka J. Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. J Exp Zool 1976; 198:155-62.
14. Sun XS, Liu Y, Yue KZ, Ma SF, Tan JH. Changes in germinal vesicle (GV) chromatin configurations during growth and maturation of porcine oocytes. Mol Reprod Dev 2004; 69:228-34.
15. Wang Q, Sun QY. Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reprod Fertil Dev 2007; 19:1-12.
16. Sun QY, Miao YL, Schatten H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 2009; 8:2741-7.
17. Bjerling P, Silverstein RA, Thon G, Caudy A, Grewal S, Ekwall K. Functional divergence between histone deacetylases in fission yeast by distinct cellular localization and in vivo specificity. Mol Cell Biol 2002; 22:2170-81.
18. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 2003; 370:737-49.
19. Akiyama T, Kim JM, Nagata M, Aoki F. Regulation of histone acetylation during meiotic maturation in mouse oocytes. Mol Reprod Dev 2004; 69:222-7.
20. Kageyama S, Liu H, Kaneko N, Ooga M, Nagata M, Aoki F. Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 2007; 133:85-94.
21. Kim JM, Liu H, Tazaki M, Nagata M, Aoki F. Changes in histone acetylation during mouse oocyte meiosis. J Cell Biol 2003; 162:37-46.
22. Nagashima T, Maruyama T, Furuya M, Kajitani T, Uchida H, Masuda H, et al. Histone acetylation and subcellular localization of chromosomal protein BRD4 during mouse oocyte meiosis and mitosis. Mol Hum Reprod 2007; 13:141-8.
23. Sarmento OF, Digilio LC, Wang Y, Perlin J, Herr JC, Allis CD, et al. Dynamic alterations of specific histone modifications during early murine development. J Cell Sci 2004; 117:4449-59. (Pubitemid 39360071)
24. Maalouf WE, Alberio R, Campbell KH. Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics 2008; 3:199-209.
25. Endo T, Naito K, Aoki F, Kume S, Tojo H. Changes in histone modifications during in vitro maturation of porcine oocytes. Mol Reprod Dev 2005; 71:123-8.
26. Wang Q, Yin S, Ai JS, Liang CG, Hou Y, Chen DY, et al. Histone deacetylation is required for orderly meiosis. Cell Cycle 2006; 5:766-74.
27. Bui HT, Van Thuan N, Kishigami S, Wakayama S, Hikichi T, Ohta H, et al. Regulation of chromatin and chromosome morphology by histone H3 modifications in pig oocytes. Reproduction 2007; 133:371-82. (Pubitemid 46359525)
28. Tang LS, Wang Q, Xiong B, Hou Y, Zhang YZ, Sun QY, et al. Dynamic changes in histone acetylation during sheep oocyte maturation. J Reprod Dev 2007; 53:555-61.
29. Polioudaki H, Markaki Y, Kourmouli N, Dialynas G, Theodoropoulos PA, Singh PB, et al. Mitotic phosphorylation of histone H3 at threonine 3. FEBS Lett 2004; 560:39-44.
30. Preuss U, Landsberg G, Scheidtmann KH. Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res 2003; 31:878-85.
31. Wang Q, Wang CM, Ai JS, Xiong B, Yin S, Hou Y, et al. Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 2006; 5:1974-82. (Pubitemid 44435304)
32. Swain JE, Ding J, Brautigan DL, Villa-Moruzzi E, Smith GD. Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity. Biol Reprod 2007; 76:628-38. (Pubitemid 46466520)
33. Gu L, Wang Q, Wang CM, Hong Y, Sun SG, Yang SY, et al. Distribution and expression of phosphorylated histone H3 during porcine oocyte maturation. Mol Reprod Dev 2008; 75:143-9. (Pubitemid 350223999)
34. Jelinkova L, Kubelka M. Neither Aurora B activity nor histone H3 phosphorylation is essential for chromosome condensation during meiotic maturation of porcine oocytes. Biol Reprod 2006; 74:905-12.
35. Bannister AJ, Schneider R, Kouzarides T. Histone methylation: dynamic or static? Cell 2002; 109:801-6.
36. Klose RJ, Zhang Y. Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 2007; 8:307-18.
37. Hou J, Liu L, Zhang J, Cui XH, Yan FX, Guan H, et al. Epigenetic modification of histone 3 at lysine 9 in sheep zygotes and its relationship with DNA methylation. BMC Dev Biol 2008; 8:60.
38. Ooga M, Inoue A, Kageyama S, Akiyama T, Nagata M, Aoki F. Changes in H3K79 methylation during preimplantation development in mice. Biol Reprod 2008; 78:413-24.
39. Park KE, Magnani L, Cabot RA. Differential remodeling of mono- and trimethylated H3K27 during porcine embryo development. Mol Reprod Dev 2009; 76:1033-42.
40. Qiao J, Chen Y, Yan LY, Yan J, Liu P, Sun QY. Changes in histone methylation during human oocyte maturation and IVF- or ICSI-derived embryo development. Fertil Steril 2009.
41. Racedo SE, Wrenzycki C, Lepikhov K, Salamone D, Walter J, Niemann H. Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation. Reprod Fertil Dev 2009; 21:738-48.
42. Wang Q, Ai JS, Idowu Ola S, Gu L, Zhang YZ, Chen DY, et al. The spatial relationship between heterochromatin protein 1alpha and histone modifications during mouse oocyte meiosis. Cell Cycle 2008; 7:513-20.
43. Pan H, O'Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol 2005; 286:493-506.
44. Yoshida N, Brahmajosyula M, Shoji S, Amanai M, Perry AC. Epigenetic discrimination by mouse metaphase II oocytes mediates asymmetric chromatin remodeling independently of meiotic exit. Dev Biol 2007; 301:464-77.
45. McGraw S, Robert C, Massicotte L, Sirard MA. Quantification of histone acetyltransferase and histone deacetylase transcripts during early bovine embryo development. Biol Reprod 2003; 68:383-9.
46. Ma P, Schultz RM. Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 2008; 319:110-20.
47. Sengupta N, Seto E. Regulation of histone deacetylase activities. J Cell Biochem 2004; 93:57-67.
48. Smillie DA, Llinas AJ, Ryan JT, Kemp GD, Sommerville J. Nuclear import and activity of histone deacetylase in Xenopus oocytes is regulated by phosphorylation. J Cell Sci 2004; 117:1857-66. (Pubitemid 38559316)
49. Kageyama S, Liu H, Nagata M, Aoki F. Stage specific expression of histone deacetylase 4 (HDAC4) during oogenesis and early preimplantation development in mice. J Reprod Dev 2006; 52:99-106.
50. Verdel A, Seigneurin-Berny D, Faure AK, Eddahbi M, Khochbin S, Nonchev S. HDAC6-induced premature chromatin compaction in mouse oocytes and fertilised eggs. Zygote 2003; 11:323-8.
51. Carrozza MJ, Utley RT, Workman JL, Cote J. The diverse functions of histone acetyltransferase complexes. Trends Genet 2003; 19:321-9.
52. Yang XJ. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res 2004; 32:959-76.
53. Thomas T, Voss AK. The diverse biological roles of MYST histone acetyltransferase family proteins. Cell Cycle 2007; 6:696-704.
54. McGraw S, Morin G, Vigneault C, Leclerc P, Sirard MA. Investigation of MYST4 histone acetyltransferase and its involvement in mammalian gametogenesis. BMC Dev Biol 2007; 7:123.
55. Endo T, Naito K, Kume S, Nishimura Y, Kashima K, Tojo H. Activities of maturation-promoting factor (MPF) and mitogen-activated protein kinase (MAPK) are not required for the global histone deacetylation observed after germinal vesicle breakdown (GVBD) in porcine oocytes. Reproduction 2006; 131:439-47.
56. Endo T, Kano K, Naito K. Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes. Biol Reprod 2008; 78:1073-80. (Pubitemid 351749290)
57. He Z, Cho YY, Ma WY, Choi HS, Bode AM, Dong Z. Regulation of ultraviolet B-induced phosphorylation of histone H3 at serine 10 by Fyn kinase. J Biol Chem 2005; 280:2446-54.
58. 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; 518:23-8.
59. Hans F, Dimitrov S. Histone H3 phosphorylation and cell division. Oncogene 2001; 20:3021-7.
60. 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 Biol 2001; 152:669-82.
61. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, Bishop DK, et al. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 2000; 102:279-91.
62. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, et al. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 2002; 22:874-85.
63. George O, Johnston MA, Shuster CB. Aurora B kinase maintains chromatin organization during the MI to MII transition in surf clam oocytes. Cell Cycle 2006; 5:2648-56. (Pubitemid 44785809)
64. 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; 7:11-7. (Pubitemid 34121301)
65. Sugiyama K, Sugiura K, Hara T, Sugimoto K, Shima H, Honda K, et al. Aurora-B associated protein phosphatases as negative regulators of kinase activation. Oncogene 2002; 21:3103-11. (Pubitemid 34548081)
66. Francisco L, Wang W, Chan CS. Type 1 protein phosphatase acts in opposition to IpL1 protein kinase in regulating yeast chromosome segregation. Mol Cell Biol 1994; 14:4731-40. (Pubitemid 24196823)
67. 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; 70:1843-51.
68. Smith CM, Haimberger ZW, Johnson CO, Wolf AJ, Gafken PR, Zhang Z, et al. Heritable chromatin structure: mapping "memory" in histones H3 and H4. Proc Natl Acad Sci USA 2002; 99:16454-61.
69. Nowak-Imialek M, Wrenzycki C, Herrmann D, Lucas-Hahn A, Lagutina I, Lemme E, et al. Messenger RNA expression patterns of histone-associated genes in bovine preimplantation embryos derived from different origins. Mol Reprod Dev 2008; 75:731-43. (Pubitemid 351438936)
70. Oliveri RS, Kalisz M, Schjerling CK, Andersen CY, Borup R, Byskov AG. Evaluation in mammalian oocytes of gene transcripts linked to epigenetic reprogramming. Reproduction 2007; 134:549-58. (Pubitemid 47555048)
71. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002; 111:185-96. (Pubitemid 35292439)
72. Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M, et al. Histone deimination antagonizes arginine methylation. Cell 2004; 118:545-53. (Pubitemid 39179708)
73. Wang Y, Wysocka J, Sayegh J, Lee YH, Perlin JR, Leonelli L, et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 2004; 306:279-83.
74. Wright PW, Bolling LC, Calvert ME, Sarmento OF, Berkeley EV, Shea MC, et al. ePAD, an oocyte and early embryo-abundant peptidylarginine deiminase-like protein that localizes to egg cytoplasmic sheets. Dev Biol 2003; 256:73-88.
75. Zuccotti M, Garagna S, Merico V, Monti M, Alberto Redi C. Chromatin organisation and nuclear architecture in growing mouse oocytes. Mol Cell Endocrinol 2005; 234:11-7. (Pubitemid 40504193)
76. De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol 2006; 292:1-12. (Pubitemid 44262111)
77. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J, et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 2005; 438:1116-22. (Pubitemid 41831675)
78. Stewart MD, Li J, Wong J. Relationship between histone H3 lysine 9 methylation, transcription repression and heterochromatin protein 1 recruitment. Mol Cell Biol 2005; 25:2525-38. (Pubitemid 40381619)
79. 2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997; 106:348-60.
80. 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; 111:3497-506. (Pubitemid 29015387)
81. 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 USA 1998; 95:7480-4. (Pubitemid 28293278)
82. Houben A, Wako T, Furushima-Shimogawara R, Presting G, Kunzel G, Schubert II, et al. Short communication: the cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J 1999; 18:675-9. (Pubitemid 29341885)
83. Gernand D, Demidov D, Houben A. The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. Cytogenet Genome Res 2003; 101:172-6.
84. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, et al. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 1999; 274:25543-9. (Pubitemid 129530724)
85. Ahn SH, Henderson KA, Keeney S, Allis CD. H2B (Ser10) phosphorylation is induced during apoptosis and meiosis in S. cerevisiae. Cell Cycle 2005; 4:780-3. (Pubitemid 41353829)
86. Barber CM, Turner FB, Wang Y, Hagstrom K, Taverna SD, Mollah S, et al. The enhancement of histone H4 and H2A serine 1 phosphorylation during mitosis and S-phase is evolutionarily conserved. Chromosoma 2004; 112:360-71. (Pubitemid 38828194)
87. Ivanovska I, Khandan T, Ito T, Orr-Weaver TL. A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev 2005; 19:2571-82. (Pubitemid 41565977)
88. Ivanovska I, Orr-Weaver TL. Histone modifications and the chromatin scaffold for meiotic chromosome architecture. Cell Cycle 2006; 5:2064-71. (Pubitemid 44553740)
89. De La Fuente R, Viveiros MM, Wigglesworth K, Eppig JJ. ATRX, a member of the SNF2 family of helicase/ATPases, is required for chromosome alignment and meiotic spindle organization in metaphase II stage mouse oocytes. Dev Biol 2004; 272:1-14. (Pubitemid 38887280)
90. Akiyama T, Nagata M, Aoki F. Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc Natl Acad Sci USA 2006; 103:7339-44. (Pubitemid 43727834)
91. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001; 2:280-91. (Pubitemid 33674776)
92. Carroll CW, Straight AF. Centromere formation: from epigenetics to self-assembly. Trends Cell Biol 2006; 16:70-8.
93. Ekwall K, Olsson T, Turner BM, Cranston G, Allshire RC. Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres. Cell 1997; 91:1021-32. (Pubitemid 28027834)
94. Taddei A, Maison C, Roche D, Almouzni G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 2001; 3:114-20. (Pubitemid 32118363)
95. Robbins AR, Jablonski SA, Yen TJ, Yoda K, Robey R, Bates SE, et al. Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 2005; 4:717-26. (Pubitemid 41353858)
96. Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999; 97:99-109. (Pubitemid 29165893)
97. Toth KF, Knoch TA, Wachsmuth M, Frank-Stohr M, Stohr M, Bacher CP, et al. Trichostatin A-induced histone acetylation causes decondensation of interphase chromatin. J Cell Sci 2004; 117:4277-87. (Pubitemid 39328314)
98. Yamashita Y, Shimada M, Harimoto N, Rikimaru T, Shirabe K, Tanaka S, et al. Histone deacetylase inhibitor trichostatin A induces cell cycle arrest/apoptosis and hepatocyte differentiation in human hepatoma cells. Int J Cancer 2003; 103:572-6. (Pubitemid 36091459)
99. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002; 419:411-5.
100. Megee PC, Morgan BA, Smith MM. Histone H4 and the maintenance of genome integrity. Genes Dev 1995; 9:1716-27.
101. Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update 2009; 15:573-85.
102. Huang JC, Yan LY, Lei ZL, Miao YL, Shi LH, Yang JW, et al. Changes in histone acetylation during postovulatory aging of mouse oocyte. Biol Reprod 2007; 77:666-70.
103. Suo L, Meng QG, Pei Y, Yan CL, Fu XW, Bunch TD, et al. Changes in acetylation on lysine 12 of histone H4 (acH4K12) of murine oocytes during maternal aging may affect fertilization and subsequent embryo development. Fertil Steril 2010; 93:945-51.