Hostname: page-component-77c89778f8-rkxrd Total loading time: 0 Render date: 2024-07-19T10:24:22.509Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro ageing of pig oocytes: effects of the histone deacetylase inhibitor trichostatin A

Published online by Cambridge University Press:  01 May 2008

M. Ješeta ,
J. Petr ,
T. Krejčová ,
E. Chmelíková  and
F. Jílek
M. Ješeta
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, University of Agriculture in Prague, Prague, Czech Republic.
J. Petr
Affiliation:
Research Institute of Animal Production, Prague, Czech Republic.
T. Krejčová*
Affiliation:
Department of Veterinary Science, Czech University of Agriculture in Prague, 165 21, Kamýcká 129, Prague 6, Czech Republic. Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, University of Agriculture in Prague, Prague, Czech Republic.
E. Chmelíková
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, University of Agriculture in Prague, Prague, Czech Republic.
F. Jílek
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, University of Agriculture in Prague, Prague, Czech Republic.
*
All correspondence to: Tereza Krejčová. Department of Veterinary Science, Czech University of Agriculture in Prague, 165 21, Kamýcká 129, Prague 6, Czech Republic. Tel.: +420 224382931. Fax: +420 234381841. e-mail: krejcova@af.czu.cz
Get access Rights & Permissions [Opens in a new window]

Summary

After in vitro maturation, the unfertilized pig oocytes underwent the process called ageing. This process involves typical events such as fragmentation, spontaneous parthenogenetic activation or lysis. Inhibition of histone deacetylase, using its specific inhibitor trichostatin A (TSA), significantly delayed the maturation of pig oocytes cultured in vitro. The ageing of oocytes matured under the effect of TSA is the same as the ageing in oocytes matured without TSA. The inhibition of histone deacetylase during oocyte ageing significantly reduced the percentage of fragmented oocytes (from 30% in untreated oocytes to 9% in oocytes aged under the effect of 100 nM of TSA). Oocytes matured in vitro and subsequently aged for 1 day under the effects of TSA retained their developmental capacity. After parthenogenetic activation, a significantly higher portion (27% vs. 15%) of oocytes developed to the blastocyst stage after 24 h ageing under 100 nM TSA when compared with oocytes activated after 24 h ageing in a TSA-free medium. The parthenogenetic development in oocytes aged under TSA treatment is similar to the development of fresh oocytes (29% of blastocyst) artificially activated immediately after in vitro maturation.

Keywords

AgeingHistone deacetylaseOocytePigTrichostatin A
Type
Research Article
Information
Zygote , Volume 16 , Issue 2 , May 2008 , pp. 145 - 152
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, J.M. & Cory, S. (1998). The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322–6.CrossRefGoogle ScholarPubMed
Akiyama, T., Kim, J.M., Nagata, M. & Aoki, F. (2004). Regulation of histone acetylation during meiotic maturation in mouse oocytes. Mol. Reprod. Dev. 69, 222–7.CrossRefGoogle ScholarPubMed
Akiyama, T., Nagata, M. & Aoki, F. (2006). Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc. Natl. Acad. Sci. USA 103, 7339–44.CrossRefGoogle ScholarPubMed
Allfrey, V.G., Faulkner, R. & Mirsky, A.E. (1964). Acetylation and methylation of histones and their possible role in regulation of RNA synthesis. Proc. Natl. Acad. Sci. USA 51, 786–94.CrossRefGoogle ScholarPubMed
Austin, C.R. (1970). Aging and reproduction: post-ovulatory deterioration of the egg. J. Reprod. Fertil. Suppl. 12, 39–53.Google ScholarPubMed
Bertos, N.R., Wang, A.H. & Yang, X.J. (2001). Class II histone deacetylases: Structure, function and regulation. Biochem. Cell. Biol. 79, 243–52.CrossRefGoogle ScholarPubMed
Bui, H.T., Thuan, N.V., Kishigami, S., Wakayama, S., Hikichi, T., Ohta, H., Mizutani, E., Yamaoka, E., Wakayama, T. & Miyano, T. (2007). Regulation of chromatin and chromosome morphology by histone H3 modifications in pig oocytes. Reproduction 133, 371–82.CrossRefGoogle ScholarPubMed
Chian, R.C., Nakahara, H., Niwa, K. & Funahashi, H. (1992). Fertilization and early cleavage in vitro of aging bovine oocytes after maturation in culture. Theriogenology 37, 665–72.CrossRefGoogle ScholarPubMed
Drexler, H.C.A. & Euler, M. (2005). Synergistic apoptosis induction by proteasome and histone deacetylase inhibitors is dependent on protein synthesis. Apoptosis 10, 743–58.CrossRefGoogle ScholarPubMed
Endo, T., Naito, K., Aoki, F., Kume, S. & Tojo, H. (2005). Changes in histone modifications during in vitro maturation of porcine oocytes. Mol. Reprod. Dev. 71, 123–8.CrossRefGoogle ScholarPubMed
Fujino, Y., Ozaki, K., Yamamasu, S., Ito, F., Matsuoka, I., Hayashi, E., Nakamura, H., Ogita, S., Sato, E. & Inoue, M. (1996). DNA fragmentation of oocytes in aged mice. Hum. Reprod. 11, 1480–3.CrossRefGoogle ScholarPubMed
Hall, V.J., Compton, D., Stojkovic, P., Nesbitt, M., Herbert, M., Murdoch, A. & Stojkovic, M. (2007). Developmental competence of human in vitro aged oocytes as host cells for nuclear transfer. Hum. Reprod. 22, 52–62.CrossRefGoogle Scholar
Ivanovska, I. & Orr-Weaver, T.L. (2006). Histone modifications and the chromatin scaffold for meiotic chromosome architecture. Cell Cycle 5, 2064–71.CrossRefGoogle ScholarPubMed
Iwamoto, M., Onishi, A., Fuchimoto, D., Somfai, T., Suzuki, S., Yazaki, S., Hashimoto, M., Takeda, K., Tagami, T., Hanada, H., Noguchi, J., Kaneko, H., Nagai, T. & Kikuchi, K. (2005). Effects of caffeine treatment on aged porcine oocytes: parthenogenetic activation ability, chromosome condensation and development to the blastocyst stage after somatic cell nuclear transfer. Zygote 13, 335–45.CrossRefGoogle Scholar
Jilek, F., Huttelova, R., Petr, J., Holubova, M. & Rozinek, J. (2001). Activation of pig oocytes using calcium ionophore: Effect of the protein kinase inhibitor 6-dimethyl aminopurine. Reprod. Domest. Anim. 36 (3–4), 139–45.Google ScholarPubMed
Jolliff, W.J. & Prather, R.S. (1997). Pathenogenic development of in vitro-matured, in vivo-cultured porcine oocytes beyond blastocyst. Biol. Reprod. 56, 544–8.CrossRefGoogle Scholar
Jurisicova, A., Lee, H.J., D'Estaing, S.G., Tilly, J. & Perez, G.I. (2006). Molecular requirements for doxorubicin-mediated death in murine oocytes. Cell Death Differ. 13, 1466–74.CrossRefGoogle ScholarPubMed
Kikuchi, K., Naito, K., Noguchi, J., Shimada, A., Kaneko, H., Yamashita, M., Tojo, H. & Toyoda, Y. (1999). Inactivation of p34cdc2 kinase by the accumulation of its phosphorylated forms in porcine oocytes matured and aged in vitro. Zygote 7, 173–9.CrossRefGoogle ScholarPubMed
Kikuchi, K., Naito, K., Noguchi, J., Shimada, A., Kaneko, H., Yamashita, M., Aoki, F., Tojo, H. & Toyoda, Y. (2000). Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biol. Reprod. 63, 715–22.CrossRefGoogle ScholarPubMed
Kim, J.M., Liu, H.L., Tazaki, M., Nagata, M. & Aoki, F. (2003). Changes in histone acetylation during mouse oocyte meiosis. J. Cell. Biol. 162, 37–46.CrossRefGoogle ScholarPubMed
Kim, N.H., Moon, S.J., Prather, R.S. & Day, B.N. (1996). Cytoskeletal alteration in aged porcine oocytes and parthenogenesis. Mol. Reprod. Dev. 43, 513–8.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Komata, T., Kanzawa, T., Nashimoto, T., Aoki, H., Endo, S., Kon, T., Takahashi, H., Kondo, S. & Tanaka, R. (2005). Histone deacetylase inhibitors, N-butyric acid and trichostatin A, induce caspase-8- but not caspase-9-dependent apoptosis in human malignant glioma cells. Int. J. Oncol. 26, 1345–52.Google Scholar
Kruhlak, M.J., Hendzel, M.J., Fischle, W., Bertos, N.R., Hameed, S., Yang, X.J., Verdin, E. & Bazett-Jones, D.P. (2001). Regulation of global acetylation in mitosis through loss of histone acetyltransferases and deacetylases from chromatin. J. Biol. Chem. 276, 38307–19.CrossRefGoogle ScholarPubMed
Marmorstein, R. & Roth, S.Y. (2001). Histone acetyltransferases: function, structure and catalysis. Curr. Opin. Genet. Dev. 11, 155–61.CrossRefGoogle ScholarPubMed
Matikainen, T., Perez, G.I., Zheng, T.S., Kluzak, T.R., Rueda, B.R., Flavell, R.A. & Tilly, J.L. (2001). Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology 142, 2468–80.CrossRefGoogle ScholarPubMed
Nagano, M., Katagiri, S. & Takahashi, Y. (2006). Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 14, 53–61.CrossRefGoogle ScholarPubMed
Nicholas, B., Alberio, R., Fouladi-Nashta, A.A. & Webb, R. (2005). Relationship between low-molecular-weight insulin-like growth factor-binding proteins, caspase-3 activity and oocyte quality. Biol. Reprod. 72, 796–804.CrossRefGoogle ScholarPubMed
Pavlok, A., Kalab, P. & Bobak, P. (1997). Fertilisation competence of bovine normally matured or aged oocytes derived from different antral follicles: morphology, protein synthesis, H1 and MBP kinase activity. Zygote 5, 235–46.CrossRefGoogle ScholarPubMed
Perez, G.I., Tao, X.J. & Tilly, J.L. (1999). Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes. Mol Hum. Reprod. 5, 414–20.CrossRefGoogle ScholarPubMed
Peters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 61.Google Scholar
Petrova, I., Sedmikova, M., Chmelikova, E., Svestkova, D. & Rajmon, R. (2004). In vitro aging of porcine oocytes. Czech J. Anim. Sci. 49, 93–8.CrossRefGoogle Scholar
Petrova, I., Rajmon, R., Sedmikova, M., Kuthanova, Z., Jilek, F. & Rozinek, J. (2005). Improvement of developmental competence of aged porcine oocytes by means of the synergistic effect of insulin-like growth factor-1 (IGF-1) and epidermal growth factor (EGF). Czech J. Anim. Sci. 50, 300–10.CrossRefGoogle Scholar
Rybouchkin, A., Kato, Y. & Tsunodaz, Y. (2006). Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biol. Reprod. 74, 1083–9.CrossRefGoogle ScholarPubMed
Sasaki, K. & Chiba, K. (2001). Fertilization blocks apoptosis of starfish eggs by inactivation of the MAP kinase pathway. Dev. Biol. 237, 18–28.CrossRefGoogle ScholarPubMed
Snedecor, G.W. & Cochran, W.G. (1980). Statistical Methods; 7th edn, pp. 1–506. Iowa: Iowa State University Press.Google Scholar
Sonnemann, H., Hartwig, M., Plath, A., Kumar, K.S., Muller, C. & Beck, J.F. (2006). Histone deacetylase inhibitors require caspase activity to induce apoptosis in lung and prostate carcinoma cells. Cancer Lett. 232, 148–60.CrossRefGoogle ScholarPubMed
Spinaci, M., Seren, E. & Mattioli, M. (2004). Maternal chromatin remodeling during maturation and after fertilization in mouse oocytes. Mol. Reprod. Dev. 69, 215–21.CrossRefGoogle ScholarPubMed
Stice, S.L., Keefer, C.L. & Matthews, L. (1994). Bovine nuclear transfer embryos: oocyte activation prior to blastomere fusion. Mol. Reprod. Dev. 38, 61–8.CrossRefGoogle ScholarPubMed
Subramanian, C., Opipari, A.W., Castle, V.P. & Kwok, R.P.S. (2005). Histone deacetylase inhibition induces apoptosis in neuroblastoma. Cell Cycle 4, 1741–3.CrossRefGoogle ScholarPubMed
Suzuki, H., Takashima, Y. & Toyokawa, K. (2002). Cytoskeletal organization of porcine oocytes aged and activated electrically or by sperm. J Reprod Dev 48, 293–301.CrossRefGoogle Scholar
Takai, N., Ueda, T., Nishida, M., Nasu, K., Matsuda, K., Kusumoto, M. & Narahara, H. (2006). CBHA is a family of hybrid polar compounds that inhibits histone deacetylase and induces growth inhibition, cell cycle arrest and apoptosis in human endometrial and ovarian cancer cells. Oncology 70, 97–105.CrossRefGoogle ScholarPubMed
Takase, K., Ishikawa, M. & Hoshiai, H. (1995). Apoptosis in the degeneration process of unfertilized mouse ova. Tohoku J. Exp. Med. 175, 69–76.CrossRefGoogle ScholarPubMed
Tanaka, H. & Kanagawa, H. (1997). Influence of combined activation treatments on the success of bovine nuclear transfer using young or aged oocytes. Anim. Reprod. Sci. 49, 113–23.CrossRefGoogle ScholarPubMed
Tarin, J.J., Perez-Albala, S. & Cano, A. (2001). Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol. Reprod. 65, 141–50.CrossRefGoogle ScholarPubMed
Tatemoto, H., Sakurai, N. & Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–10.CrossRefGoogle ScholarPubMed
Toth, K.F., Knoch, T.A., Wachsmuth, M., Frank-Stohr, M., Stohr, M., Bacher, C.P., Muller, G. & Rippe, K. (2004). Trichostatin A-induced histone acetylation causes decondensation of interphase chromatin. J. Cell Sci. 117, 4277–87.CrossRefGoogle ScholarPubMed
Wang, A.G., Kim, S.U., Lee, S.H., Kim, S.K., Seo, S.B., Yu, D.Y. & Lee, D.S. (2005). Histone deacetylase 1 contributes to cell cycle and apoptosis. Biol. Pharm. Bull. 28, 1966–70.CrossRefGoogle ScholarPubMed
Wang, Q., Wang, C.M., Ai, J.S., Xiong, B., Yin, S., Hou, Y., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2006a). Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 5, 1974–82.CrossRefGoogle ScholarPubMed
Wang, Q., Yin, S., Ai, J.S., Liang, C.G., Hou, Y., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2006b). Histone deacetylation is required for orderly meiosis. Cell Cycle 5, 766–74.CrossRefGoogle ScholarPubMed
Wassarman, P.M. (1988). The mammalian ovum. In The Physiology of Reproduction; (eds Knobil, E. & Neil, J.), pp. 69–102. New York: Raven Press.Google Scholar
Wetzel, M., Premkumar, D.R.D., Arnold, B. & Pollack, I.F. (2005). Effect of trichostatin A, a histone deacetylase inhibitor, on glioma proliferation in vitro by inducing cell cycle arrest and apoptosis. J. Neurosurg. 103, 549–56.Google ScholarPubMed
Yamashita, Y., Shimada, M., Harimoto, N., Rikimaru, T., Shirabe, K., Tanaka, S. & Sugimachi, K. (2003). Histone, deacetylase inhibitor trichostatin A induces cell-cycle arrest/apoptosis and hepatocyte differentiation in human hepatoma cells. Int. J. Cancer 103, 572–6.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1988). Mammalian fertilization. In The Physiology of Reproduction; (eds Knobil, E. & Neil, J.), pp. 135–85. New York: Raven Press.Google Scholar
Yoshida, M. & Beppu, T (1988). Reversible arrest of proliferation of rat 3Y1 fibroblasts in both the G1-phase and G2-phase by trichostatin-A. Exp Cell Res 177, 122–31.CrossRefGoogle ScholarPubMed
Yüce, O. & Sadler, K.C. (2001). Postmeiotic unfertilized starfish eggs die by apoptosis. Dev. Biol. 237, 29–44.CrossRefGoogle ScholarPubMed