Theriogenology
Volume 74, Issue 9 , Pages 1539-1547 , December 2010

Aging changes the chromatin configuration and histone methylation of mouse oocytes at germinal vesicle stage

  • I. Manosalva

      Affiliations

    • Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid, Spain
    • Corresponding Author InformationCorresponding author: Current address: Institute for Virus Research, Kyoto University, 53 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto, Japan. Tel.: +81-75-751-4013; fax: +81-75-751-4807
  • ,
  • A. González

      Affiliations

    • Institute for Virus Research, Kyoto University, 53 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto, Japan

Received 3 March 2010 ,Revised 26 May 2010 ,Accepted 21 June 2010.

References 

  1. Ottolenghi C, Uda M, Hamatani T, Crisponi L, Garcia JE, Ko M, et al. Aging of oocyte, ovary, and human reproduction. Ann N Y Acad Sci. 2004;1034:117–131
  2. Zuccotti M, Piccinelli A, Giorgi Rossi P, Garagna S, Redi CA. Chromatin organization during mouse oocyte growth. Mol Reprod Dev. 1995;41:479–485
  3. Christians E, Boiani M, Garagna S, Dessy C, Redi CA, Renard JP, et al. Gene expression and chromatin organization during mouse oocyte growth. Dev Biol. 1999;207:76–85
  4. Debey P, Szollosi MS, Szollosi D, Vautier D, Girousse A, Besombes D. Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol Reprod Dev. 1993;36:59–74
  5. Mattson BA, Albertini DF. Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev. 1990;25:374–383
  6. Tarin JJ, Perez-Albala S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod. 2001;65:141–150
  7. Eichenlaub-Ritter U. Genetics of oocyte ageing. Maturitas. 1998;30:143–169
  8. Zuccotti M, Boiani M, Garagna S, Redi CA, Eichenlaub-Ritter U. Analysis of aneuploidy rate in antral and ovulated mouse oocytes during female aging. Mol Reprod Dev. 1998;50:305–312
  9. Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, et al. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet. 2004;13:2263–2278
  10. 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;77:666–670
  11. Liang XW, Zhu JQ, Miao YL, Liu JH, Wei L, Lu SS, et al. Loss of methylation imprint of Snrpn in postovulatory aging mouse oocyte. Biochem Biophys Res Commun. 2008;371:16–21
  12. 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;103:7339–7344
  13. Manosalva I, Gonzalez A. Aging alters histone H4 acetylation and CDC2A in mouse germinal vesicle stage oocytes. Biol Reprod. 2009;81:1164–1171
  14. 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;117:4449–4459
  15. 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
  16. Ooga M, Inoue A, Kageyama S, Akiyama T, Nagata M, Aoki F. Changes in H3K79 Methylation During Preimplantation Development in Mice. Biol Reprod. 2008;78:413–424
  17. Sedivy JM, Banumathy G, Adams PD. Aging by epigenetics—a consequence of chromatin damage?. Exp Cell Res. 2008;314:1909–1917
  18. Obuse C, Iwasaki O, Kiyomitsu T, Goshima G, Toyoda Y, Yanagida M. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat Cell Biol. 2004;6:1135–1141
  19. Rangasamy D, Greaves I, Tremethick DJ. RNA interference demonstrates a novel role for H2A.Z in chromosome segregation. Nat Struct Mol Biol. 2004;11:650–655
  20. Zhang R, Adams PD. Heterochromatin and its relationship to cell senescence and cancer therapy. Cell Cycle. 2007;6:784–789
  21. Anastasiou D, Krek W. SIRT1: linking adaptive cellular responses to aging-associated changes in organismal physiology. Physiology (Bethesda). 2006;21:404–410
  22. Sasaki T, Maier B, Bartke A, Scrable H. Progressive loss of SIRT1 with cell cycle withdrawal. Aging Cell. 2006;5:413–422
  23. Vaquero A, Scher M, Erdjument-Bromage H, Tempst P, Serrano L, Reinberg D. SIRT1 regulates the histone methyl-transferase SUV39H1 during heterochromatin formation. Nature. 2007;450:440–444
  24. Tarin JJ, Perez-Albala S, Cano A. Consequences on offspring of abnormal function in ageing gametes. Hum Reprod Update. 2000;6:532–549
  25. Zuccotti M, Giorgi Rossi P, Martinez A, Garagna S, Forabosco A, Redi CA. Meiotic and developmental competence of mouse antral oocytes. Biol Reprod. 1998;58:700–704
  26. De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol. 2006;292:1–12
  27. Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szollosi MS, Debey P. Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol Reprod. 1999;60:580–587
  28. Longo F, Garagna S, Merico V, Orlandini G, Gatti R, Scandroglio R, et al. Nuclear localization of NORs and centromeres in mouse oocytes during folliculogenesis. Mol Reprod Dev. 2003;66:279–290
  29. Andux S, Ellis RE. Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females. PLoS Genet. 2008;4:e1000295
  30. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature. 2001;410:120–124
  31. Arney KL, Fisher AG. Epigenetic aspects of differentiation. J Cell Sci. 2004;117:4355–4363
  32. De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, Eppig JJ. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol. 2004;275:447–458
  33. Li J, Lin Q, Yoon HG, Huang ZQ, Strahl BD, Allis CD, et al. Involvement of histone methylation and phosphorylation in regulation of transcription by thyroid hormone receptor. Mol Cell Biol. 2002;22:5688–5697
  34. Calvanese V, Lara E, Kahn A, Fraga MF. The role of epigenetics in aging and age-related diseases. Ageing Res Rev. 2009;8:268–276
  35. Jacquet P. Sensitivity of germ cells and embryos to ionizing radiation. J Biol Regul Homeost Agents. 2004;18:106–114
  36. Gonzalo S, Blasco MA. Role of Rb family in the epigenetic definition of chromatin. Cell Cycle. 2005;4:752–755
  37. Sanders SL, Portoso M, Mata J, Bahler J, Allshire RC, Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell. 2004;119:603–614
  38. Arney KL, Bao S, Bannister AJ, Kouzarides T, Surani MA. Histone methylation defines epigenetic asymmetry in the mouse zygote. Int J Dev Biol. 2002;46:317–320
  39. Meglicki M, Zientarski M, Borsuk E. Constitutive heterochromatin during mouse oogenesis: the pattern of histone H3 modifications and localization of HP1alpha and HP1beta proteins. Mol Reprod Dev. 2008;75:414–428
  40. Zhang R, Liu ST, Chen W, Bonner M, Pehrson J, Yen TJ, et al. HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells. Mol Cell Biol. 2007;27:949–962

PII: S0093-691X(10)00342-0

doi: 10.1016/j.theriogenology.2010.06.024

Theriogenology
Volume 74, Issue 9 , Pages 1539-1547 , December 2010