Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 8, 2012, Pages

  Ma, Pengpeng ^a   Pan, Hua ^a   Montgomery, Rusty L ^b   Olson, Eric N ^b   Schultz, Richard M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; TRANSCRIPTOME;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; FEMALE; FEMALE INFERTILITY; GENE DELETION; GERMINAL VESICLE; HISTONE ACETYLATION; HISTONE METHYLATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

ACETYLATION; ANIMALS; APOPTOSIS; DNA-BINDING PROTEINS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONES; HYDROXAMIC ACIDS; INFERTILITY, FEMALE; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; LYSINE; METHYLATION; MICE; OOCYTES; OOGENESIS; ORGAN SIZE; OVARIAN FOLLICLE; RNA INTERFERENCE; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84857428826     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1118403109     Document Type: Article

References (68)

1. Rodrigues P, Limback D, McGinnis LK, Plancha CE, Albertini DF (2008) Oogenesis: Prospects and challenges for the future. J Cell Physiol 216:355-365. (Pubitemid 351898462)
2. van den Hurk R, Zhao J (2005) Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63:1717-1751.
3. Moore GP, Lintern-Moore S (1978) Transcription of the mouse oocyte genome. Biol Reprod 18:865-870. (Pubitemid 8368134)
4. De La Fuente R, Eppig JJ (2001) Transcriptional activity of the mouse oocyte genome: Companion granulosa cells modulate transcription and chromatin remodeling. Dev Biol 229:224-236. (Pubitemid 32061726)
5. Kageyama S, et al. (2007) Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 133:85-94. (Pubitemid 46332158)
6. Bhaumik SR, Smith E, Shilatifard A (2007) Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 14:1008-1016. (Pubitemid 350060343)
7. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074-1080. (Pubitemid 32758077)
8. Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349-352.
9. Hubbert C, et al. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417:455-458. (Pubitemid 34563539)
10. Luo J, Su F, Chen D, Shiloh A, Gu W (2000) Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408:377-381.
11. Martínez-Balbás MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T (2000) Regulation of E2F1 activity by acetylation. EMBO J 19:662-671. (Pubitemid 30093739)
12. Minucci S, Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6:38-51. (Pubitemid 43054973)
13. Bolden JE, Peart MJ, Johnstone RW (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5:769-784. (Pubitemid 44348499)
14. Brunmeir R, Lagger S, Seiser C (2009) Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int J Dev Biol 53:275-289.
15. Mehnert JM, Kelly WK (2007) Histone deacetylase inhibitors: Biology and mechanism of action. Cancer J 13:23-29.
16. Haberland M, Montgomery RL, Olson EN (2009) The many roles of histone deacetylases in development and physiology: Implications for disease and therapy. Nat Rev Genet 10:32-42.
17. Grozinger CM, Schreiber SL (2002) Deacetylase enzymes: Biological functions and the use of small-molecule inhibitors. Chem Biol 9:3-16. (Pubitemid 34155860)
18. Montgomery RL, et al. (2007) Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21:1790-1802. (Pubitemid 47076478)
19. Montgomery RL, Hsieh J, Barbosa AC, Richardson JA, Olson EN (2009) Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci USA 106:7876-7881.
20. Yamaguchi T, et al. (2010) Histone deacetylases 1 and 2 act in concert to promote the G1-to-S progression. Genes Dev 24:455-469.
21. LeBoeuf M, et al. (2010) Hdac1 and Hdac2 act redundantly to control p63 and p53 functions in epidermal progenitor cells. Dev Cell 19:807-818.
22. Lagger G, et al. (2002) Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21:2672-2681. (Pubitemid 34619383)
23. Guan JS, et al. (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459:55-60.
24. Dovey OM, Foster CT, Cowley SM (2010) Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc Natl Acad Sci USA 107:8242-8247.
25. Ma P, Schultz RM (2008) Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 319:110-120.
26. Lan ZJ, et al. (2003) GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO J 22:4070-4081.
27. Lewandoski M, Wassarman KM, Martin GR (1997) Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr Biol 7:148-151. (Pubitemid 27155624)
28. Epifano O, Liang L-F, Familari M, Moos MC, Jr., Dean J (1995) Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development 121:1947-1956.
29. Lira SA, Kinloch RA, Mortillo S, Wassarman PM (1990) An upstream region of the mouse ZP3 gene directs expression of firefly luciferase specifically to growing oocytes in transgenic mice. Proc Natl Acad Sci USA 87:7215-7219.
30. Haberland M, Mokalled MH, Montgomery RL, Olson EN (2009) Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev 23:1625-1630.
31. Yang XJ, Seto E (2008) Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 31:449-461.
32. Ma P, Lin S, Bartolomei MS, Schultz RM (2010) Metastasis tumor antigen 2 (MTA2) is involved in proper imprinted expression of H19 and Peg3 during mouse preimplantation development. Biol Reprod 83:1027-1035.
33. Taunton J, Hassig CA, Schreiber SL (1996) A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272:408-411. (Pubitemid 26138177)
34. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407-412.
35. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41-45. (Pubitemid 30038513)
36. Shilatifard A (2006) Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annu Rev Biochem 75:243-269.
37. Hublitz P, Albert M, Peters AH (2009) Mechanisms of transcriptional repression by histone lysine methylation. Int J Dev Biol 53:335-354.
38. Ni Z, Schwartz BE, Werner J, Suarez JR, Lis JT (2004) Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol Cell 13:55-65. (Pubitemid 38117115)
39. Hengartner CJ, et al. (1998) Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol Cell 2:43-53. (Pubitemid 128378965)
40. Komarnitsky P, Cho EJ, Buratowski S (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14:2452-2460.
41. Andreu-Vieyra CV, et al. (2010) MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol 8:e1000453.
42. Wysocka J, et al. (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121:859-872. (Pubitemid 40806418)
43. Yamane K, et al. (2007) PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell 25:801-812. (Pubitemid 46436533)
44. O'Connor L, et al. (1998) Bim: A novel member of the Bcl-2 family that promotes apoptosis. EMBO J 17:384-395. (Pubitemid 28045479)
45. Chao DT, Korsmeyer SJ (1998) BCL-2 family: Regulators of cell death. Annu Rev Immunol 16:395-419. (Pubitemid 28183370)
46. Vaux DL (1998) Immunopathology of apoptosis - introduction and overview. Springer Semin Immunopathol 19:271-278.
47. Janumyan YM, et al. (2003) Bcl-xL/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry. EMBO J 22:5459-5470. (Pubitemid 37279955)
48. el-Deiry WS, et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
49. Haupt S, Berger M, Goldberg Z, Haupt Y (2003) Apoptosis - the p53 network. J Cell Sci 116:4077-4085. (Pubitemid 37337082)
50. Ito A, et al. (2002) MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J 21:6236-6245. (Pubitemid 35415340)
51. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W (2008) Acetylation is indispensable for p53 activation. Cell 133:612-626. (Pubitemid 351636297)
52. Nagashima M, et al. (2001) DNA damage-inducible gene p33ING2 negatively regulates cell proliferation through acetylation of p53. Proc Natl Acad Sci USA 98:9671-9676. (Pubitemid 32769361)
53. Su YQ, Sugiura K, Eppig JJ (2009) Mouse oocyte control of granulosa cell development and function: Paracrine regulation of cumulus cell metabolism. Semin Reprod Med 27:32-42.
54. McNatty KP, et al. (2005) Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129:481-487. (Pubitemid 40542174)
55. Scibetta AG, et al. (2007) Functional analysis of the transcription repressor PLU-1/JARID1B. Mol Cell Biol 27:7220-7235. (Pubitemid 47549757)
56. Tan K, et al. (2003) Human PLU-1 Has transcriptional repression properties and interacts with the developmental transcription factors BF-1 and PAX9. J Biol Chem 278:20507-20513. (Pubitemid 36806347)
57. Gazdag E, et al. (2009) TBP2 is essential for germ cell development by regulating transcription and chromatin condensation in the oocyte. Genes Dev 23:2210-2223.
58. Pan H, O'brien MJ, Wigglesworth K, Eppig JJ, Schultz RM (2005) Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol 286:493-506.
59. Sorensen RA, Wassarman PM (1976) Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol 50:531-536.
60. Freedman DA, Wu L, Levine AJ (1999) Functions of the MDM2 oncoprotein. Cell Mol Life Sci 55:96-107. (Pubitemid 29077858)
61. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ (2010) Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366-369.
62. Tsafriri A, Chun S-Y, Zhang R, Hsueh AJW, 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 178:393-402. (Pubitemid 26365046)
63. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I (1989) An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 86:679-688. (Pubitemid 19183391)
64. Svoboda P, Stein P, Schultz RM (2001) RNAi in mouse oocytes and preimplantation embryos: Effectiveness of hairpin dsRNA. Biochem Biophys Res Commun 287:1099-1104. (Pubitemid 32980565)
65. Whitten WK (1971) Nutrient requirements for the culture of preimplantation mouse embryo in vitro. Adv Biosci 6:129-139.
66. Aoki F, Worrad DM, Schultz RM (1997) Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 181:296-307. (Pubitemid 27089080)
67. Zeng F, Baldwin DA, Schultz RM (2004) Transcript profiling during preimplantation mouse development. Dev Biol 272:483-496. (Pubitemid 38988270)
68. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.