Abstract
Trichostatin A (TSA), a histone deacetylase inhibitor, is a known teratogen causing malformations such as vertebral fusions when applied during the postimplantation period; TSA also causes developmental arrest when applied during the preimplantation period. Regardless of these hindrances, we have succeeded in the establishment of an efficient somatic cloning method for the mouse where reconstructed embryos are treated with TSA. To elucidate this apparent discrepancy, we treated fertilized mouse embryos generated either by intracytoplasmic sperm injection (ICSI) or round spermatid injection (ROSI) with 50 nM TSA for 20 h after fertilization as well as parthenogenetic embryos and found that TSA treatment inhibited the preimplantation development of ICSI embryos but not ROSI or parthenogenetic embryos. And, although we often observed hypomorphism following TSA treatment in embryos grown to full term produced by both ICSI (av. of body weight: 1.7 g vs. 1.5 g) and ROSI (1.6 g vs. 1.2 g), TSA treatment reduced the offspring production rate for ICSI from 57% to 34% but not for ROSI from 30% to 36%. Thus, these data indicate that the effects, harmful or not, of TSA treatment on embryonic development depend on their nuclear derivations. Also, the resulting hypomorphism after TSA treatment is a caveat for this procedure in current Assisted Reproductive Technologies.
[1] T. Wakayama, A.C.F. Perry, M. Zuccotti, K.R. Johnson and R. Yanagimachi: “Fullterm development of mice from enucleated oocytes injected with cumulus cell nuclei”, Nature, Vol. 394, (1998), pp. 369–374. http://dx.doi.org/10.1038/2861510.1038/28615Search in Google Scholar PubMed
[2] H. Kishikawa, T. Wakayama and R. Yanagimachi: “Comparison of oocyte-activating agents for mouse cloning”, Cloning, Vol. 1, (1999), pp. 153–159. http://dx.doi.org/10.1089/1520455995001991510.1089/15204559950019915Search in Google Scholar PubMed
[3] T. Wakayama and R. Yanagimachi: “Effect of cytokinesis inhibitor, DMSO and the timing of oocyte activation on mouse cloning using cumulus cell nuclei”, Reproduction, Vol. 122, (2001), pp. 49–60. http://dx.doi.org/10.1530/rep.0.122004910.1530/rep.0.1220049Search in Google Scholar PubMed
[4] S. Wakayama, E. Mizutani, S. Kishigami, N.V. Thuan, H. Ohta, T. Hikichi, H.T. Bui, M. Miyake and T. Wakayama: “Mice cloned by nuclear transfer from somatic and ntES cells derived from the same individuals”, J. Reprod. Dev., Vol. 51, (2005), pp. 765–772. http://dx.doi.org/10.1262/jrd.1706110.1262/jrd.17061Search in Google Scholar PubMed
[5] S. Wakayama, J.B. Cibelli and T. Wakayama: “Effect of timing of the removal of oocyte chromosomes before or after injection of somatic nucleus on development of NT embryos”, Cloning Stem Cells, Vol. 5, (2003), pp. 181–189. http://dx.doi.org/10.1089/15362300376964584810.1089/153623003769645848Search in Google Scholar PubMed
[6] S. Kishigami, E. Mizutani, H. Ohta, T. Hikichi, N. Van Thuan, S. Wakayama, H.T. Bui and T. Wakayama: “Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer”, Biochem. Biophys. Res. Commun., Vol. 340, (2006), pp. 183–189. http://dx.doi.org/10.1016/j.bbrc.2005.11.16410.1016/j.bbrc.2005.11.164Search in Google Scholar PubMed
[7] A. Rybouchkin, Y. Kato and Y. Tsunoda: “Role of Histone Acetylation in Reprogramming of Somatic Nuclei Following Nuclear Transfer”, Biol. Reprod., Vol. 74, (2006), pp. 1083–1089. http://dx.doi.org/10.1095/biolreprod.105.04745610.1095/biolreprod.105.047456Search in Google Scholar PubMed
[8] S. Kishigami, S. Wakayama, N. Van Thuan, H. Ohta, E. Mizutani, T. Hikichi, H.T. Bui, S. Balbach, A Ogura, M. Boiani and T. Wakayama: “Production of Cloned Mice by Somatic Cell Nuclear Transfer”, Nat. Protocols, Vol. 1, (2006), pp. 125–138. http://dx.doi.org/10.1038/nprot.2006.2110.1038/nprot.2006.21Search in Google Scholar PubMed
[9] S. Kishigami, N. Van Thuan, T. Hikichi, H. Ohta, S. Wakayama, E. Mizutani and T. Wakayama: “Epigenetic abnormalities of the mouse paternal zygotic genome associated with microinsemination of round spermatids”, Dev. Biol., Vol. 289, (2006), pp. 195–205. http://dx.doi.org/10.1016/j.ydbio.2005.10.02610.1016/j.ydbio.2005.10.026Search in Google Scholar PubMed
[10] A. Ogura, J. Matsuda and R. Yanagimachi: “Birth of normal young after electrofusion of mouse oocytes with round spermatids”, Proc. Natl. Acad. Sci. U.S.A., Vol. 91, (1994), pp. 7460–7462. http://dx.doi.org/10.1073/pnas.91.16.746010.1073/pnas.91.16.7460Search in Google Scholar PubMed PubMed Central
[11] Y. Kimura and R. Yanagimachi: “Mouse oocytes injected with testicular spermatozoa or round spermatids can develop int normal offspring”, Development, Vol. 121, (1995), pp. 2397–2405. Search in Google Scholar
[12] S. Kishigami, S. Wakayama, N. Van Thuan and T. Wakayama: “Similar time restriction for intracytoplasmic sperm injection and round spermatid injection into activated oocytes for efficient offspring production”, Biol. Reprod., Vol. 70, (2004), pp. 1863–1869. http://dx.doi.org/10.1095/biolreprod.103.02517110.1095/biolreprod.103.025171Search in Google Scholar
[13] S. Kishigami, N. Van Thuan, S. Wakayama, T. Hikichi and T. Wakayama: “A novel method for isolating spermatid nuclei from cytoplasm prior to ROSI in the mouse”, Zygote, Vol. 12, (2004), pp. 321–327. http://dx.doi.org/10.1017/S096719940400296510.1017/S0967199404002965Search in Google Scholar
[14] R. Yanagimachi: “Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in human and animals”, Reprod. Biomed. Online, Vol. 10, (2005), pp. 247–286. http://dx.doi.org/10.1016/S1472-6483(10)60947-910.1016/S1472-6483(10)60947-9Search in Google Scholar
[15] J. Ohgane, T. Wakayama, S. Senda, Y. Yamazaki, K. Inoue, A. Ogura, J. Marh, S. Tanaka, R. Yanagimachi and K. Shiota: “The Sall3 locus is an epigenetic hotspot of aberrant DNA methylation associated with placentomegaly of cloned mice”, Genes Cells, Vol. 9, (2004), pp. 253–260. http://dx.doi.org/10.1111/j.1356-9597.2004.00720.x10.1111/j.1356-9597.2004.00720.xSearch in Google Scholar
[16] Y.K. Kang, D.B. Koo, J.S. Park, Y.H. Choi, A.S. Chung, K.K. Lee and Y.M. Han: “Aberrant methylation of donor genome in cloned bovine embryos”, Nat. Genet., Vol. 28, (2001), pp. 173–177. http://dx.doi.org/10.1038/8890310.1038/88903Search in Google Scholar
[17] W. Dean, F. Santos, M. Stojkovic, V. Zakhartchenko, J. Walter, E. Wolf, and W. Reik: “Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos”, Proc. Natl. Acad. Sci. U.S.A., Vol. 98, (2001), pp. 13734–13738. http://dx.doi.org/10.1073/pnas.24152269810.1073/pnas.241522698Search in Google Scholar
[18] F. Santos, V. Zakhartchenko, M. Stojkovic, A. Peters, T. Jenuwein, E. Wolf, W. Reik and W. Dean: “Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos”, Curr. Biol., Vol. 13, (2003), pp. 1116–1121. http://dx.doi.org/10.1016/S0960-9822(03)00419-610.1016/S0960-9822(03)00419-6Search in Google Scholar
[19] M. Dokmanovic and P.A. Marks: “Prospects: histone deacetylase inhibitors”, J. Cell Biochem., Vol. 96, (2005), pp. 293–304. http://dx.doi.org/10.1002/jcb.2053210.1002/jcb.20532Search in Google Scholar PubMed
[20] N. Gurvich, M.G. Berman, B.S. Wittner, R.C. Gentleman, P.S. Klein and J.B. Green: “Association of valproate-induced teratogenesis with histone deacetylase inhibition in vivo”, FASEB J., Vol. 19, (2005), pp. 1166–1168. Search in Google Scholar
[21] K. Svensson, R. Mattsson, T.C. James, P. Wentzel, M. Pilartz, J. MacLaughlin, S.J. Miller, T. Olsson, U.J. Eriksson and R. Ohlsson: “The paternal allele of the H19 gene is progressively silenced during early mouse development: the acetylation status of histones may be involved in the generation of variegated expression patterns”, Development, Vol. 125, (1998), pp. 61–69. Search in Google Scholar
[22] M. Yoshida, M. Kijima, M. Akita and T. Beppu: “Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A”, J. Biol. Chem., Vol. 265, (1990), pp. 17174–17179. Search in Google Scholar
[23] J. Ma, P. Svoboda, R.M. Schultz and P. Stein: “Regulation of zygotic gene activation in the preimplantation mouse embryo: global activation and repression of gene expression”, Biol. Reprod., Vol. 64, (2001), pp. 1713–1721. http://dx.doi.org/10.1095/biolreprod64.6.171310.1095/biolreprod64.6.1713Search in Google Scholar PubMed
[24] G.T. O’Neill, L.R. Rolfe and M.H. Kaufman: “Developmental potential and chromosome constitution of strontium-induced mouse parthenogenones”, Mol. Reprod. Dev., Vol. 30, (1991), pp. 214–219. http://dx.doi.org/10.1002/mrd.108030030810.1002/mrd.1080300308Search in Google Scholar PubMed
[25] M. Spinaci, E. Seren and M. Mattioli: “Maternal chromatin remodeling during maturation and after fertilization in mouse oocytes”, Mol. Reprod. Dev., Vol. 69, (2004), pp. 215–221. http://dx.doi.org/10.1002/mrd.2011710.1002/mrd.20117Search in Google Scholar PubMed
[26] B.P. Enright, C. Kubota, X. Yang, and X.C. Tian: “Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2’-deoxycytidine”, Biol. Reprod., Vol. 69, (2003), pp. 896–901. http://dx.doi.org/10.1095/biolreprod.103.01795410.1095/biolreprod.103.017954Search in Google Scholar PubMed
[27] M. Szyf: “DNA methylation and demethylation as targets for anticancer therapy”, Biochemistry (Mosc), Vol. 70, (2005), pp. 533–549. http://dx.doi.org/10.1007/s10541-005-0147-710.1007/s10541-005-0147-7Search in Google Scholar PubMed
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