Histone Deacetylase 2 (HDAC2) Regulates Chromosome Segregation and Kinetochore Function via H4K16 Deacetylation during Oocyte Maturation in Mouse

English version České info

Changes in histone acetylation occur during oocyte development and maturation, but the role of specific histone deacetylases in these processes is poorly defined. We report here that mice harboring Hdac1^−/+/Hdac2^−/− or Hdac2^−/− oocytes are infertile or sub-fertile, respectively. Depleting maternal HDAC2 results in hyperacetylation of H4K16 as determined by immunocytochemistry—normal deacetylation of other lysine residues of histone H3 or H4 is observed—and defective chromosome condensation and segregation during oocyte maturation occurs in a sub-population of oocytes. The resulting increased incidence of aneuploidy likely accounts for the observed sub-fertility of mice harboring Hdac2^−/− oocytes. The infertility of mice harboring Hdac1^−/+/Hdac2^−/−oocytes is attributed to failure of those few eggs that properly mature to metaphase II to initiate DNA replication following fertilization. The increased amount of acetylated H4K16 likely impairs kinetochore function in oocytes lacking HDAC2 because kinetochores in mutant oocytes are less able to form cold-stable microtubule attachments and less CENP-A is located at the centromere. These results implicate HDAC2 as the major HDAC that regulates global histone acetylation during oocyte development and, furthermore, suggest HDAC2 is largely responsible for the deacetylation of H4K16 during maturation. In addition, the results provide additional support that histone deacetylation that occurs during oocyte maturation is critical for proper chromosome segregation.

Vyšlo v časopise: Histone Deacetylase 2 (HDAC2) Regulates Chromosome Segregation and Kinetochore Function via H4K16 Deacetylation during Oocyte Maturation in Mouse. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003377
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003377

Souhrn

Zdroje

1. KouzaridesT (2007) Chromatin modifications and their function. Cell 128 : 693–705.

2. IizukaM, SmithMM (2003) Functional consequences of histone modifications. Curr Opin Genet Dev 13 : 154–160.

3. JenuweinT, AllisCD (2001) Translating the histone code. Science 293 : 1074–1080.

4. de RuijterAJ, van GennipAH, CaronHN, KempS, van KuilenburgAB (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370 : 737–749.

5. BrunmeirR, LaggerS, SeiserC (2009) Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int J Dev Biol 53 : 275–289.

6. LeBoeufM, TerrellA, TrivediS, SinhaS, EpsteinJA, et al. (2010) Hdac1 and Hdac2 act redundantly to control p63 and p53 functions in epidermal progenitor cells. Dev Cell 19 : 807–818.

7. MontgomeryRL, DavisCA, PotthoffMJ, HaberlandM, FielitzJ, et al. (2007) Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21 : 1790–1802.

8. MontgomeryRL, HsiehJ, BarbosaAC, RichardsonJA, OlsonEN (2009) Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci U S A 106 : 7876–7881.

9. YamaguchiT, CubizollesF, ZhangY, ReichertN, KohlerH, et al. (2010) Histone deacetylases 1 and 2 act in concert to promote the G1-to-S progression. Genes Dev 24 : 455–469.

10. DoveyOM, FosterCT, CowleySM (2010) Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc Natl Acad Sci U S A 107 : 8242–8247.

11. GuanJS, HaggartySJ, GiacomettiE, DannenbergJH, JosephN, et al. (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459 : 55–60.

12. LaggerG, O'CarrollD, RemboldM, KhierH, TischlerJ, et al. (2002) Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. Embo J 21 : 2672–2681.

13. MaP, SchultzRM (2008) Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 319 : 110–120.

14. MaP, PanH, MontgomeryRL, OlsonEN, SchultzRM (2012) Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proc Natl Acad Sci, USA 109: E481–489.

15. ZuccottiM, PonceRH, BoianiM, GuizzardiS, GovoniP, et al. (2002) The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote 10 : 73–78.

16. StrahlBD, AllisCD (2000) The language of covalent histone modifications. Nature 403 : 41–45.

17. BergerSL (2007) The complex language of chromatin regulation during transcription. Nature 447 : 407–412.

18. NiZ, SchwartzBE, WernerJ, SuarezJR, LisJT (2004) Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol Cell 13 : 55–65.

19. YamaneK, TateishiK, KloseRJ, FangJ, FabrizioLA, et al. (2007) PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell 25 : 801–812.

20. ItoA, KawaguchiY, LaiCH, KovacsJJ, HigashimotoY, et al. (2002) MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J 21 : 6236–6245.

21. TangY, ZhaoW, ChenY, ZhaoY, GuW (2008) Acetylation is indispensable for p53 activation. Cell 133 : 612–626.

22. De La FuenteR, ViveirosMM, WigglesworthK, EppigJJ (2004) 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 272 : 1–14.

23. KimJM, LiuH, TazakiM, NagataM, AokiF (2003) Changes in histone acetylation during mouse oocyte meiosis. J Cell Biol 162 : 37–46.

24. SarmentoOF, DigilioLC, WangY, PerlinJ, HerrJC, et al. (2004) Dynamic alterations of specific histone modifications during early murine development. J Cell Sci 117 : 4449–4459.

25. EndoT, NaitoK, AokiF, KumeS, TojoH (2005) Changes in histone modifications during in vitro maturation of porcine oocytes. Mol Reprod Dev 71 : 123–128.

26. TaipaleM, ReaS, RichterK, VilarA, LichterP, et al. (2005) hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol Cell Biol 25 : 6798–6810.

27. SmithER, CayrouC, HuangR, LaneWS, CoteJ, et al. (2005) A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Mol Cell Biol 25 : 9175–9188.

28. RobbinsAR, JablonskiSA, YenTJ, YodaK, RobeyR, et al. (2005) Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 4 : 717–726.

29. ChoyJS, AcunaR, AuWC, BasraiMA (2011) A role for histone H4K16 hypoacetylation in Saccharomyces cerevisiae kinetochore function. Genetics 189 : 11–21.

30. RiederCL (1981) The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 84 : 145–158.

31. AngerM, SteinP, SchultzRM (2005) CDC6 requirement for spindle formation during maturation of mouse oocytes. Biol Reprod 72 : 188–194.

32. MuraiS, SteinP, BuffoneMG, YamashitaS, SchultzRM (2010) Recruitment of Orc6l, a dormant maternal mRNA in mouse oocytes, is essential for DNA replication in 1-cell embryos. Dev Biol 341 : 205–212.

33. SuYQ, SugiuraK, EppigJJ (2009) Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Seminars in reproductive medicine 27 : 32–42.

34. PanH, O'Brien MJ, WigglesworthK, EppigJJ, SchultzRM (2005) Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol 286 : 493–506.

35. LanZJ, GuP, XuX, JacksonKJ, DeMayoFJ, et al. (2003) GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO J 22 : 4070–4081.

36. DebeyP, SzollosiMS, SzollosiD, VautierD, GirousseA, et al. (1993) Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Molecular reproduction and development 36 : 59–74.

37. ZuccottiM, PiccinelliA, Giorgi RossiP, GaragnaS, RediCA (1995) Chromatin organization during mouse oocyte growth. Molecular reproduction and development 41 : 479–485.

38. BurnsKH, ViveirosMM, RenY, WangP, DeMayoFJ, et al. (2003) Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300 : 633–636.

39. Andreu-VieyraCV, ChenR, AgnoJE, GlaserS, AnastassiadisK, et al. (2010) MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol 8: e1000453 doi:10.1371/journal.pbio.1000453

40. KageyamaS, LiuH, KanekoN, OogaM, NagataM, et al. (2007) Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 133 : 85–94.

41. LiuJ, McConnellK, DixonM, CalviBR Analysis of model replication origins in Drosophila reveals new aspects of the chromatin landscape and its relationship to origin activity and the prereplicative complex. Mol Biol Cell 23 : 200–212.

42. ChristiansE, DavisAA, ThomasSD, BenjaminIJ (2000) Maternal effect of Hsf1 on reproductive success. Nature 407 : 693–694.

43. PayerB, SaitouM, BartonSC, ThresherR, DixonJP, et al. (2003) Stella is a maternal effect gene required for normal early development in mice. Curr Biol 13 : 2110–2117.

44. WuX, WangP, BrownCA, ZilinskiCA, MatzukMM (2003) Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol Reprod 69 : 861–867.

45. TongZB, GoldL, PfeiferKE, DorwardH, LeeE, et al. (2000) Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 26 : 267–268.

46. VaqueroA, SternglanzR, ReinbergD (2007) NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs. Oncogene 26 : 5505–5520.

47. EndoT, KanoK, NaitoK (2008) Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes. Biol Reprod 78 : 1073–1080.

48. AkiyamaT, NagataM, AokiF (2006) Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc Natl Acad Sci U S A 103 : 7339–7344.

49. Shogren-KnaakM, IshiiH, SunJM, PazinMJ, DavieJR, et al. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311 : 844–847.

50. RobbinsAR, JablonskiSA, YenTJ, YodaK, RobeyR, et al. (2005) Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 4 : 717–726.

51. ChiangT, DuncanFE, SchindlerK, SchultzRM, LampsonMA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20 : 1522–1528.

52. van den BergIM, EleveldC, van der HoevenM, BirnieE, SteegersEA, et al. (2011) Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment. Hum Reprod 26 : 1181–1190.

53. ChatotCL, ZiomekCA, BavisterBD, LewisJL, TorresI (1989) An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. Journal of Reproduction and Fertility 86 : 679–688.

54. KurasawaS, SchultzRM, KopfGS (1989) Egg-induced modifications of the zona pellucida of mouse eggs: effects of microinjected inositol 1,4,5-trisphosphate. Dev Biol 133 : 295–304.

55. WhittenWK (1971) Nutrient requirements for the culture of preimplantation mouse embryo in vitro. Adv Biosci 6 : 129–139.

56. MainigiMA, OrdT, SchultzRM (2011) Meiotic and developmental competence in mice are compromised following follicle development in vitro using an alginate-based culture system. Biol Reprod 85 : 269–276.

57. HoY, WigglesworthK, EppigJJ, SchultzRM (1995) Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol Reprod Dev 41 : 232–238.

58. AokiF, WorradDM, SchultzRM (1997) Regulation of transcriptional activity during the first and second cell cycles in the preimplanation mouse embryo. Dev Biol 181 : 296–307.