Skip to main content
SpringerLink
Log in

Fully-mature antral mouse oocytes are transcriptionally silent but their heterochromatin maintains a transcriptional permissive histone acetylation profile

  • Gamete Biology
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

The final stages of antral mouse oocytes maturation are characterised by the transition from transcriptionally active NSN to inactive SN oocytes. Here, we studied the profile of histone acetylation changes occurring during the NSN-to-SN transition.

Methods

During the NSN-to-SN transition, oocytes were classified based on their chromatin organisation and the immunocytochemical profile of histones H2B, H3 and H4 acetylation was analysed.

Results

We described four patterns of immunostaining common to the three acetylated histones, corresponding to stages of progressive localisation: From a diffused distribution in NSN oocytes to the association with constitutive heterochromatin and then to the nucleolar surface region in SN oocytes.

Conclusions

The maintenance of a favourable transcriptional epigenetic context, in the heterochromatin of transcriptionally silent SN oocytes, might be related to the early stages of development when transcripts from these heterochromatic regions are functional to preimplantation progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szollosi MS, Debey P. Differential transcriptional activity associated to chromatin configuration in fully grown germinal vesicle mouse oocytes. Biol Reprod. 1999;60:580–7.

    Article  PubMed  CAS  Google Scholar 

  2. 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.

    Article  PubMed  CAS  Google Scholar 

  3. Chambeyron S, Bickmore WA. Does looping and clustering in the nucleus regulate gene expression? Curr Opin Cell Biol. 2004;16:256–62.

    Article  PubMed  CAS  Google Scholar 

  4. 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.

    Article  PubMed  CAS  Google Scholar 

  5. Debey P, Szollozi MS, Szollosi D, Vautier D, Girouse A, Besombes D. Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Molec Reprod Dev. 1993;36:59–74.

    Article  PubMed  CAS  Google Scholar 

  6. De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol. 2006;292:1–12.

    Article  Google Scholar 

  7. 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;275:447–58.

    Article  Google Scholar 

  8. Foygel K, Choi B, Jun S, Leong DE, Lee A, Wong CC, et al. A novel and critical role for Oct4 as a regulator of the maternal-embryonic transition. PLoS One. 2008;3(12):e4109.

    Article  PubMed  Google Scholar 

  9. Inoue A, Nakajima R, Nagata M, Aoki F. Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Human Reprod. 2008;23:1377–84.

    Article  CAS  Google Scholar 

  10. 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.

    Article  PubMed  CAS  Google Scholar 

  11. Kaplan G, Abreu S, Bachvarova R. rRNA accumulation and protein synthetic patterns in growing mouse oocytes. J Exp Zool. 1982;220:361–70.

    Article  PubMed  CAS  Google Scholar 

  12. 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.

    Article  PubMed  CAS  Google Scholar 

  13. Li L, Zheng P, Dean J. Maternal control of early mouse development. Development. 2010;137:859–70.

    Article  PubMed  CAS  Google Scholar 

  14. Liu H, Aoki F. Transcription activity associated with meiotic competence in fully grown mouse GV oocytes. Zygote. 2002;10:327–32.

    PubMed  CAS  Google Scholar 

  15. 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;66:279–90.

    Article  PubMed  CAS  Google Scholar 

  16. Mattson DA, Albertini DF. Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev. 1990;25:374–83.

    Article  PubMed  CAS  Google Scholar 

  17. Miyara F, Migne C, Dumont-Hassan M, Le Meur A, Cohen-Bacrie P, Aubriot F, et al. Chromatin configuration and transcriptional control in human and mouse oocytes. Mol Reprod Dev. 2003;64:458–70.

    Article  PubMed  CAS  Google Scholar 

  18. Moore GPM, Lintern-Moore S, Peters H, Faber M. RNA synthesis in the mouse oocyte. J Cell Biol. 1974;60:416–22.

    Article  PubMed  CAS  Google Scholar 

  19. Ola SI, Wang Q, Ai JS, Yin S, Liang CG, Chen DY, et al. Meiotic competence and acetylation pattern of UV light classified mouse antral oocytes after meiotic arrest with isobutylmethylxanthine. Mol Reprod Dev. 2007;74:591–9.

    Article  PubMed  CAS  Google Scholar 

  20. Payer B, Saitou M, Barton SC, Thresher R, Dixon JPC, Zahn D, et al. Stella is a maternal effect gene required for normal early development in mice. Current Biol. 2003;13:2110–7.

    Article  CAS  Google Scholar 

  21. Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell. 2010;19:625–38.

    Article  PubMed  CAS  Google Scholar 

  22. Shi L, Wu J. Epigenetic regulation in mammalian preimplantation embryo development. Reprod Biol Endocrinol. 2009;7:59–70.

    Article  PubMed  Google Scholar 

  23. Tan J, Wang H, Sun X, Liu Y, Sui H, Zhang J. Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol Hum Reprod. 2009;15:1–9.

    Article  PubMed  CAS  Google Scholar 

  24. Zuccotti M, Piccinelli A, Giorgi Rossi P, Garagna S, Redi CA. Chromatin organization during mouse oocyte growth. Mol Reprod Dev. 1995;41:479–85.

    Article  PubMed  CAS  Google Scholar 

  25. Zuccotti M, Ponce RH, Boiani M, Guizzardi S, Govoni P, Scandroglio R, et al. The analysis of chromatin organization allows selection of mouse antral oocytes competent for development to blastocyst. Zygote. 2002;10:73–8.

    Article  PubMed  Google Scholar 

  26. Zuccotti M, Garagna S, Merico V, Monti M, Redi CA. Chromatin organisation and nuclear architecture in growing mouse oocytes. Mol Cell Endocrinol. 2005;234:11–7.

    Article  PubMed  CAS  Google Scholar 

  27. Zuccotti M, Merico V, Sacchi L, Bellone M, Brink TC, Bellazzi R, et al. Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes. BMC Dev Biol. 2008;8:97.

    Article  PubMed  Google Scholar 

  28. Zuccotti M, Merico V, Sacchi L, Bellone M, Brink TC, Stefanelli M, et al. Oct-4 regulates the expression of Stella and Foxj2 at the Nanog locus: implications for the developmental competence of mouse oocytes. Human Reprod. 2009;24:2225–37.

    Article  CAS  Google Scholar 

  29. Zuccotti M, Merico V, Redi CA, Garagna S (2011) What does it take to make a mammalian developmentally competent oocyte? Human Reprod. Update; in press

Download references

Acknowledgements

We thank the following organisations for supporting this research: University of Parma (FIL), UNIPV-Regione Lombardia, Fondazione Alma Mater Ticinensis, Fondazione I.R.C.C.S. Policlinico San Matteo , and ‘Bando Giovani Ricercatori 2007’ to C.A.R.

Author information

Authors and Affiliations

  1. Sezione di Istologia ed Embriologia, Dipartimento di Medicina Sperimentale, Universita’ degli Studi di Parma, Parma, Italy

    Maurizio Zuccotti

  2. Laboratorio di Biologia dello Sviluppo, Dipartimento di Biologia Animale, Universita’ degli Studi di Pavia, Pavia, Italy

    Michele Bellone, Carlo Alberto Redi & Silvia Garagna

  3. Department of Anatomy, University of Iowa, Iowa, IA, USA

    Frank Longo

  4. Fondazione I.R.C.C.S. Policlinico San Matteo, Pavia, Italy

    Carlo Alberto Redi

  5. Centro di Ingegneria Tissutale, and Centro di Eccellenza in Biologia Applicata, Universita’ degli Studi di Pavia, Pavia, Italy

    Silvia Garagna

  6. Dipartimento di Medicina Sperimentale, Sezione di Istologia ed Embriologia, Via Volturno 39, 43100, Parma, Italy

    Maurizio Zuccotti

  7. Dipartimento di Biologia Animale, Laboratorio di Biologia dello Sviluppo, Via Ferrata 9, 27100, Pavia, Italy

    Silvia Garagna

Authors
  1. Maurizio Zuccotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michele Bellone
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frank Longo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlo Alberto Redi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Silvia Garagna
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Maurizio Zuccotti or Silvia Garagna.

Additional information

Capsule In late antral mouse oocytes, chromatin condenses around the nucleolus, becomes transcriptionally silent, but maintains transcriptionally permissive histone acetylation profiles, likely functional to development.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zuccotti, M., Bellone, M., Longo, F. et al. Fully-mature antral mouse oocytes are transcriptionally silent but their heterochromatin maintains a transcriptional permissive histone acetylation profile. J Assist Reprod Genet 28, 1193–1196 (2011). https://doi.org/10.1007/s10815-011-9562-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-011-9562-4

Keywords

Search

Navigation