Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T14:12:05.715Z Has data issue: false hasContentIssue false
  • English
  • Français

Enhancement of histone acetylation by trichostatin A during in vitro fertilization of bovine oocytes affects cell number of the inner cell mass of the resulting blastocysts

Published online by Cambridge University Press:  01 August 2009

Shuntaro Ikeda ,
Atsuhiro Tatemizo ,
Daisaku Iwamoto ,
Shunji Taniguchi ,
Yoichiro Hoshino ,
Tomoko Amano ,
Kazuya Matsumoto ,
Yoshihiko Hosoi ,
Akira Iritani  and
Kazuhiro Saeki
Shuntaro Ikeda
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Atsuhiro Tatemizo
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Daisaku Iwamoto
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Shunji Taniguchi
Affiliation:
Wakayama Prefecture Livestock Experimental Station, Wakayama, Japan.
Yoichiro Hoshino
Affiliation:
Gifu Prefectural Livestock Research Institute, Gifu, Japan.
Tomoko Amano
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Kazuya Matsumoto
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Yoshihiko Hosoi
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Akira Iritani
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, Japan.
Kazuhiro Saeki*
Affiliation:
Department of Genetic Engineering, Kinki University, Wakayama, 6496493, Japan. Department of Genetic Engineering, Kinki University, Wakayama, Japan.
*
All correspondence to: Kazuhiro Saeki. Department of Genetic Engineering, Kinki University, Wakayama, 6496493, Japan. Tel: +81 736 77 3888. Fax: +81 736 77 4754. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Histone acetylation is one of the major mechanisms of epigenetic reprogramming of gamete genomes after fertilization to establish a totipotent state for normal development. In the present study, the effects of trichostatin A (TSA), an inhibitor of histone deacetylase, during in vitro fertilization (IVF) of bovine oocytes on subsequent embryonic development were investigated. Cumulus-enclosed oocytes obtained from slaughterhouse bovine ovaries were matured in vitro and subjected to IVF in a defined medium supplemented with 0 (control), 5, 50, and 500 nM TSA for 18 h. After IVF, presumptive zygotes were cultured in modified synthetic oviductal fluid (mSOF) medium until 168 h postinsemination (hpi). Some oocytes were immunostained using antibody specific for histone H4-acetylated lysine 5 at 10 hpi. Cleavage, blastocyst development and cell number of inner cell mass (ICM) and trophectoderm (TE) of blastocysts were assessed. TSA treatment enhanced histone acetylation that was prominent in decondensed sperm nuclei. TSA did not affect the postfertilization cleavage, blastocyst rates, and TE cell number. However, it significantly enhanced ICM cell number (p < 0.05). These results indicate that TSA treatment during IVF of bovine oocytes does not affect blastocyst development but alters the cell number of ICM, suggesting that overriding epigenetic modification of the genome during fertilization has a carryover effect on cell proliferation and differentiation in preimplantation embryos. Thus, further environmental quality controls in assisted reproductive technologies are needed in terms of factors which affect chromatin remodelling.

Keywords

BlastocystsChromatin remodellingHistone acetylationIn vitro fertilizationTrichostatin A
Type
Research Article
Information
Zygote , Volume 17 , Issue 3 , August 2009 , pp. 209 - 215
Copyright
Copyright © Cambridge University Press 2009

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

Adenot, P.G., Mercier, Y., Renard, J.P. & Thompson, E.M. (1997). Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124, 4615–25.CrossRefGoogle ScholarPubMed
Bird, A.P. & Wolffe, A.P. (1999). Methylation-induced repression-belts, braces, and chromatin. Cell 99, 451–4.Google Scholar
Brackett, B.G. & Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–74.Google Scholar
Brison, D.R. & Schultz, R.M. (1997). Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol. Reprod. 56, 1088–96.CrossRefGoogle ScholarPubMed
Cervoni, N. & Szyf, M. (2001). Demethylase activity is directed by histone acetylation. J. Biol. Chem. 276, 40778–87.CrossRefGoogle ScholarPubMed
Ekwall, K., Olsson, T., Turner, B.M., Cranston, G. & Allshire, R.C. (1997). Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres. Cell 91, 1021–32.Google Scholar
Gioia, L., Barboni, B., Turriani, M., Capacchietti, G., Pistilli, M.G., Berardinelli, P. & Mattioli, M. (2005) The capability of reprogramming the male chromatin after fertilization is dependent on the quality of oocyte maturation. Reproduction 130, 29–39.Google Scholar
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Statis. 6, 65–70.Google Scholar
Jenuwein, T. & Allis, C.D. (2001). Translating the histone code. Science 293, 1074–80.CrossRefGoogle ScholarPubMed
Kang, Y.K., Park, J.S., Koo, D.B., Choi, Y.H., Kim, S.U., Lee, K.K. & Han, Y.M. (2002). Limited demethylation leaves mosaic-type methylation states in cloned bovine pre-implantation embryos. EMBO J. 21, 1092–100.CrossRefGoogle ScholarPubMed
Kasamatsu, A., Saeki, K., Tamari, T., Iwamoto, D., Tatemizo, A., Matsumoto, K., Hosoi, Y. & Iritani, A. (2007). Timing and uniformity of embryonic gene activation affect subsequent pre-implantation development of cloned bovine embryos. J. Reprod. Dev. 53, 623–9.Google Scholar
Kishigami, S., Thuan, N.V., Hikichi, T., Ohta, H., Wakayama, S., Mizutani, E. & Wakayama, T. (2006a). Epigenetic abnormalities of the mouse paternal zygotic genome associated with microinsemination of round spermatids. Dev. Biol. 289, 195–205.Google Scholar
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N.V., Wakayama, S., Bui, H.T. & Wakayama, T. (2006b). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–9.Google Scholar
Koo, D.B., Kang, Y.K., Choi, Y.H., Park, J.S., Kim, H.N., Oh, K.B., Son, D.S., Park, H., Lee, K.K. & Han, Y.M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol. Reprod. 67, 487–92.CrossRefGoogle ScholarPubMed
Maalouf, W.E., Alberio, R. & Campbell, K.H. (2008). Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics 3, 199–209.CrossRefGoogle ScholarPubMed
McGraw, S., Robert, C., Massicotte, L. & Sirard, M. A. (2003). Quantification of histone acetyltransferase and histone deacetylase transcripts during early bovine embryo development. Biol. Reprod. 68, 383–9.CrossRefGoogle ScholarPubMed
McLay, D.W. & Clarke, H.J. (2003). Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125, 625–33.Google Scholar
Mizzen, C.A. & Allis, C.D. (1998). Linking histone acetylation to transcriptional regulation. Cell. Mol. Life Sci. 54, 6–20.Google Scholar
Perreault, S.D. (1992). Chromatin remodeling in mammalian zygotes. Mutat. Res. 296, 43–55.CrossRefGoogle ScholarPubMed
Rybouchkin, A., Kato, Y. & Tsunoda, Y. (2006). Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biol. Reprod. 74, 1083–9.CrossRefGoogle ScholarPubMed
Saeki, K., Hoshi, M., Leibfried-Rutledge, M.L. & First, N.L. (1990). In vitro fertilization and development of bovine oocytes matured with commercially available follicle stimulating hormone. Theriogenology 34, 1035–9.Google Scholar
Saeki, K., Kato, H., Hosoi, Y., Miyake, M., Utsumi, K. & Iritani, A. (1991). Early morphological events of in vitro fertilized bovine oocytes with frozen–thawed spermatozoa. Theriogenology 35, 1051–8.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.Google Scholar
Takahashi, Y. & First, N.L. (1992). In vitro development of bovine one-cell embryos: Influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology 37, 963–78.Google Scholar
Tarin, J.J., Perez-Albala, S., Gomez-Piquer, V., Hermenegildo, C. & Cano, A. (2002). Stage of the estrous cycle at the time of pregnant mare's serum gonadotropin injection affects pre-implantation embryo development in vitro in the mouse. Mol. Reprod. Dev. 62, 312–9.Google Scholar
Thouas, G.A., Korfiatis, N.A., French, A.J., Jones, G.M. & Trounson, A.O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3, 25–9.CrossRefGoogle ScholarPubMed
Torres-Padilla, M.E., Parfitt, D.E., Kouzarides, T. & Zernicka-Goetz, M. (2007). Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214–8.CrossRefGoogle ScholarPubMed
Turner, B.M. (1998). Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell. Mol. Life Sci. 54, 21–31.Google Scholar
Turner, B.M. (2000). Histone acetylation and an epigenetic code. Bioessays 22, 836–45.Google Scholar
Turner, B.M. (2002). Cellular memory and the histone code. Cell 111, 285–91.CrossRefGoogle ScholarPubMed
Ward, W.S. & Coffey, D.S. (1991). DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44, 569–74.CrossRefGoogle ScholarPubMed
Ward, W.S. & Zalensky, A.O. (1996). The unique, complex organization of the transcriptionally silent sperm chromatin. Crit. Rev. Eukaryot. Gene Expr. 6, 139–47.CrossRefGoogle ScholarPubMed
Wee, G., Koo, D.B., Song, B.S., Kim, J.S., Kang, M.J., Moon, S.J., Kang, Y.K., Lee, K.K. & Han, Y.M. (2006). Inheritable histone H4 acetylation of somatic chromatins in cloned embryos. J. Biol. Chem. 281, 6048–57.CrossRefGoogle ScholarPubMed